The human protein kinase HIPK2 phosphorylates and downregulates the methyl-binding transcription factor ZBTB4

Oncogene

Volumn 28, Issue 27, 2009, Pages 2535-2544

  Yamada, D ^a   Perez Torrado R ^a   Filion, G ^a   Caly, M ^a   Jammart, B ^a   Devignot, V ^a   Sasai, N ^a,d   Ravassard, P ^b   Mallet, J ^b   Sastre Garau, X ^a   Schmitz, M L ^c   Defossez, P A ^a,d  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d Université Sorbonne Paris Cité   (France)

Author keywords

Epigenetics; Protein kinase; Transcription

Indexed keywords

HOMEODOMAIN INTERACTING PROTEIN KINASE 2; MUTANT PROTEIN; PROTEIN P53; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZBTB4; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; CONTROLLED STUDY; DNA DAMAGE; DNA METHYLATION; DOWN REGULATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SEQUENCE; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; CELL LINE, TUMOR; DNA DAMAGE; DOWN-REGULATION; HCT116 CELLS; HUMANS; IMMUNOPRECIPITATION; LUMINESCENT PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUTATION; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; THREONINE; TWO-HYBRID SYSTEM TECHNIQUES;

EUKARYOTA;

EID: 67650447715     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.109     Document Type: Article

References (40)

1. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP et al. (1998). Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282: 1497-1501.
2. Calzado MA, Renner F, Roscic A, Schmitz ML. (2007). HIPK2: a Versatile Switchboard Regulating the Transcription Machinery and Cell Death. Cell Cycle 6: 139-143.
3. Clouaire T, Stancheva I. (2008). Methyl-CpG bindingproteins: specialized transcriptional repressors or structural components of chromatin? Cell Mol Life Sci 65: 1509-1522.
4. D'Orazi G, Cecchinelli B, Bruno T, Manni I, Higashimoto Y, Saito S et al. (2002). Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat Cell Biol 4: 11-19.
5. Dauth I, Kruger J, Hofmann TG. (2007). Homeodomain-interacting protein kinase 2 is the ionizingradiation-activated p53 serine 46 kinase and is regulated by ATM. Cancer Res 67: 2274-2279.
6. Defossez PA, Kelly KF, Filion GJ, Perez-Torrado R, Magdinier F, Menoni H et al. (2005). The human enhancer blocker CTC-binding factor interacts with the transcription factor Kaiso. J Biol Chem 280: 43017-43023.
7. Deshmukh H, Yeh TH, Yu J, Sharma MK, Perry A, Leonard JR et al. (2008). High-resolution, dual-platform aCGH analysis reveals frequent HIPK2 amplification and increased expression in pilocytic astrocytomas. Oncogene 27: 4745-4751.
8. Di Stefano V, Rinaldo C, Sacchi A, Soddu S, D'Orazi G. (2004). Homeodomain-interacting protein kinase-2 activity and p53 phosphorylation are critical events for cisplatin-mediated apoptosis. Exp Cell Res 293: 311-320.
9. Di Stefano V, Soddu S, Sacchi A, D'Orazi G. (2005). HIPK2 contributes to PCAF-mediated p53 acetylation and selective transactivation of p21Waf1 after nonapoptotic DNA damage. Oncogene 24: 5431-5442.
10. Engelhardt OG, Boutell C, Orr A, Ullrich E, Haller O, Everett RD. (2003). The homeodomain-interactingkinase PKM (HIPK-2) modifies ND10 through both its kinase domain and a SUMO-1 interaction motif and alters the posttranslational modification of PML. Exp Cell Res 283: 36-50.
11. Filion GJ, Fouvry L, Defossez PA. (2006a). Usingreverse electrophoretic mobility shift assay to measure and compare protein-DNA bindingaffinities. Anal Biochem 357: 156-158.
12. Filion GJ, Zhenilo S, Salozhin S, Yamada D, Prokhortchouk E, Defossez PA. (2006b). A family of human zinc finger proteins that bind methylated DNA and repress transcription. Mol Cell Biol 26: 169-181.
13. Gresko E, Roscic A, Ritterhoff S, Vichalkovski A, del Sal G, Schmitz ML. (2006). Autoregulatory control of the p53 response by caspase-mediated processing of HIPK2. Embo J 25: 1883-1894.
14. Hofmann TG, Moller A, Sirma H, Zentgraf H, Taya Y, Droge W et al. (2002). Regulation of p53 activity by its interaction with home-odomain- interacting protein kinase-2. Nat Cell Biol 4: 1-10.
15. Isono K, Nemoto K, Li Y, Takada Y, Suzuki R, Katsuki M et al. (2006). Overlappingroles for homeodomain-interacting protein kinases hipk1 and hipk2 in the mediation of cell growth in response to morphogenetic and genotoxic signals. Mol Cell Biol 26: 2758-2771.
16. James P, Halladay J, Craig EA. (1996). Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144: 1425-1436.
17. Kanduri C, Fitzpatrick G, Mukhopadhyay R, Kanduri M, Lobanenkov V, Higgins M et al. (2002). A differentially methylated imprintingcontrol region within the Kcnq1 locus harbours a methylation-sensitive chromatin insulator. J Biol Chem 4: 4.
18. Kelly KF, Daniel JM. (2006). POZ for effect-POZ-ZF transcription factors in cancer and development. Trends Cell Biol 16: 578-587.
19. Lee W, Swarup S, Chen J, Ishitani T, Verheyen EM. (2009). Homeodomain-interacting protein kinases (Hipks) promote Wnt/Wgsignali. Development 136: 241-251.
20. Li XL, Arai Y, Harada H, Shima Y, Yoshida H, Rokudai S et al. (2007). Mutations of the HIPK2 gene in acute myeloid leukemia and myelodysplastic syndrome impair AML1- and p53-mediated transcription. Oncogene 26: 7231-7239.
21. Moller A, Sirma H, Hofmann TG, Staege H, Gresko E, Ludi KS et al. (2003). Sp100 is important for the stimulatory effect of home-odomain- interacting protein kinase-2 on p53-dependent gene expression. Oncogene 22: 8731-8737.
22. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T et al. (2000). p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102: 849-862.
23. Ovcharenko D, Jarvis R, Hunicke-Smith S, Kelnar K, Brown D. (2005). High-throughput RNAi screening in vitro: from cell lines to primary cells. RNA 11: 985-993.
24. Perez-Torrado R, Yamada D, Defossez PA. (2006). Born to bind: the BTB protein-protein interaction domain. Bioessays 28: 1194-1202.
25. Phan RT, Saito M, Basso K, Niu H, Dalla-Favera R. (2005). BCL6 interacts with the transcription factor Miz-1 to suppress the cyclin-dependent kinase inhibitor p21 and cell cycle arrest in germinal center B cells. Nat Immunol 6: 1054-1060.
26. Pierantoni GM, Fedele M, Pentimalli F, Benvenuto G, Pero R, Viglietto G et al. (2001). High mobility group I (Y) proteins bind HIPK2, a serine-threonine kinase protein which inhibits cell growth. Oncogene 20: 6132-6141.
27. Pierantoni GM, Rinaldo C, Mottolese M, Di Benedetto A, Esposito F, Soddu S et al. (2007). High-mobility group A1 inhibits p53 by cytoplasmic relocalization of its proapoptotic activator HIPK2. J Clin Invest 117: 693-702.
28. Rinaldo C, Prodosmo A, Mancini F, Iacovelli S, Sacchi A, Moretti F et al. (2007a). MDM2-regulated degradation of HIPK2 prevents p53Ser46 phosphorylation and DNA damage-induced apoptosis. Mol Cell 25: 739-750.
29. Rinaldo C, Prodosmo A, Siepi F, Soddu S. (2007b). HIPK2: a multitalented partner for transcription factors in DNA damage response and development. Biochem Cell Biol 85: 411-418.
30. Rinaldo C, Siepi F, Prodosmo A, Soddu S. (2008). HIPKs: Jack of all trades in basic nuclear activities. Biochim Biophys Acta 1783: 2124-2129.
31. Roscic A, Moller A, Calzado MA, Renner F, Wimmer VC, Gresko E et al. (2006). Phosphorylation-dependent control of Pc2 SUMO E3 ligase activity by its substrate protein HIPK2. Mol Cell 24: 77-89.
32. Rui Y, Xu Z, Lin S, Li Q, Rui H, Luo W et al. (2004). Axin stimulates p53 functions by activation of HIPK2 kinase through multimeric complex formation. Embo J 23: 4583-4594.
33. Tomasini R, Samir AA, Carrier A, Isnardon D, Cecchinelli B, Soddu S et al. (2003). TP53INP1 s and homeodomain-interacting protein kinase-2 (HIPK2) are partners in regulating p53 activity. J Biol Chem 278: 37722-37729.
34. van Roy FM, McCrea PD. (2005). A role for Kaiso-p120ctn complexes in cancer? Nat Rev Cancer 5: 956-964.
35. Weber A, Marquardt J, Elzi D, Forster N, Starke S, Glaum A et al. (2008). Zbtb4 represses transcription of P21CIP1 and controls the cellular response to p53 activation. EMBO J 27: 1563-1574.
36. Wei G, Ku S, Ma GK, Saito S, Tang AA, ZhangJ et al. (2007). HIPK2 represses beta-catenin-mediated transcription, epidermal stem cell expansion, and skin tumorigenesis. Proc Natl Acad Sci USA 104: 13040-13045.
37. Wesierska-Gadek J, Schmitz ML, Ranftler C. (2007). Roscovitine-activated HIP2 kinase induces phosphorylation of wt p53 at Ser-46 in human MCF-7 breast cancer cells. J Cell Biochem 100: 865-874.
38. Zhang Q, Nottke A, Goodman RH. (2005). Homeodomain-interacting protein kinase-2 mediates CtBP phosphorylation and degradation in UV-triggered apoptosis. Proc Natl Acad Sci USA 102: 2802-2807.
39. Zhang Q, Wang Y. (2007). Homeodomain-interacting protein kinase-2 (HIPK2) phosphorylates HMGA1a at Ser-35, Thr-52, and Thr-77 and modulates its DNA bindingaffinity. J Proteome Res 6: 4711-4719.
40. Zhang Q, Yoshimatsu Y, Hildebrand J, Frisch SM, Goodman RH. (2003). Homeodomain interacting protein kinase 2 promotes apoptosis by downregulating the transcriptional corepressor CtBP. Cell 115: 177-186.