Overlapping roles for homeodomain-interacting protein kinases Hipk1 and Hipk2 in the mediation of cell growth in response to morphogenetic and genotoxic signals

Molecular and Cellular Biology

Volumn 26, Issue 7, 2006, Pages 2758-2771

  Isono, Kyoichi ^a   Nemoto, Kazumi ^a   Li, Yuanyuan ^b   Takada, Yuki ^a   Suzuki, Rie ^a   Katsuki, Motoya ^c   Nakagawara, Akira ^b   Koseki, Haruhiko ^a  

^a RIKEN Center for Integrative Medical Sciences   (Japan)

^b CHIBA CANCER CENTER   (Japan)

^c NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; HOMEODOMAIN INTERACTING PROTEIN KINASE 1; HOMEODOMAIN INTERACTING PROTEIN KINASE 2; LUCIFERASE; PROTEIN SERINE THREONINE KINASE; RNA; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; EXENCEPHALY; FEMALE; GENOTOXICITY; HOMOZYGOTE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MALE; MESODERM; MORPHOGENESIS; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CARRIER PROTEINS; CELL CYCLE; CELL GROWTH PROCESSES; CELL PROLIFERATION; CELLS, CULTURED; EMBRYO LOSS; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; HOMOZYGOTE; MESODERM; MICE; MORPHOGENESIS; MUTAGENS; NEURAL TUBE DEFECTS; NEURONS; PAIRED BOX TRANSCRIPTION FACTORS; PROTEIN BINDING; PROTEIN KINASES; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; ERINACEIDAE;

EID: 33645238760     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.7.2758-2771.2006     Document Type: Article

References (69)

1. Akasaka, T., M. Kanno, R. Balling, M. A. Mieza, M. Taniguchi, and H. Koseki. 1996. A role for Mel18, a Polycomb group-related vertebrate gene, during the anteroposterior specification of the axial skeleton. Development 122:1513-1522.
2. Akimaru, H., Y. Chen, P. Dai, D. X. Hou, M. Nonaka, S. M. Smolik, S. Armstrong, R. H. Goodman, and S. Ishii. 1997. Drosophila CBP is a co-activator of cubitus interruptus in hedgehog signalling. Nature 386:735-738.
3. Armstrong, J. F., M. H. Kaufman, D. J. Harrison, and A. R. Clarke. 1995. High-frequency developmental abnormalities in p53-deficient mice. Curr. Biol. 5:931-936.
4. Bergson, C., and W. McGinnis. 1990. An autoregulatory enhancer element of the Drosophila homeotic gene Deformed. EMBO J. 9:4287-4297.
5. Chen, Z. F., and R. R. Behringer. 1995. Twist is required in head mesenchyme for cranial neural tube morphogenesis. Gene Dev. 9:689-699.
6. Chiang, C., Y. Litingtung, E. Lee, K. E. Young, J. L. Corden, H. Westphal, and P. A. Beachy. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383:407-413.
7. Choi, C. Y., Y. H. Kim, H. J. Kwon, and Y. Kim. 1999. The homeodomain protein NK-3 recruits Groucho and a historic deacetylase complex to repress transcription. J. Biol. Chem. 274:33194-33197.
8. Cordenonsi, M., S. Dupont, S. Maretto, A. Insinga, C. Imbriano, and S. Piccolo. 2003. Links between tumor suppressors: p53 is required for TGF-beta gene responses by cooperating with Smads. Cell 113:301-314.
9. Dai, P., H. Akimaru, Y. Tanaka, T. Maekawa, M. Nakafuku, and S. Ishii. 1999. Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274:8143-8152.
10. Diez del Corral, R., and K. G. Storey. 2004. Opposing FGF and retinoid pathways: a signalling switch that controls differentiation and patterning onset in the extending vertebrate body axis. Bioessays 26:857-869.
11. Di Stefano, V., G. Blandino, A. Sacchi, S. Soddu, and G. D'Orazi. 2004. HIPK2 neutralizes MDM2 inhibition rescuing p53 transcriptional activity and apoptotic function. Oncogene 23:5185-5192.
12. Di Stefano, V., C. Rinaldo, A. Sacchi, S. Soddu, and G. D'Orazi. 2004. Homeodomain-interacting protein kinase-2 activity and p53 phosphorylation are critical events for cisplatin-mediated apoptosis. Exp. Cell Res. 293:311-320.
13. Di Stefane, V., S. Soddu, A. Sacchi, and G. D'Orazi. 2005. HIPK2 contributes to PCAF-mediated p53 acetylation and selective transactivation of p21(Waf1) after nonapoptotic DNA damage. Oncogene 24:5431-5442.
14. D'Orazi, G., B. Cecchinelli, T. Bruno, I. Manni, Y. Higashimoto, S. Saito, M. Gostissa, S. Coen, A. Marchetti, G. Del Sal, G. Piaggio, M. Fanciulli, E. Appella, and S. Soddu. 2002. Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat. Cell Biol. 4:11-19.
15. Doxakis, E., E. J. Huang, and A. M. Davies. 2004. Homeodomain-interacting protein kinase-2 regulates apoptosis in developing sensory and sympathetic neurons. Curr. Biol. 14:1761-1765.
16. Ecsedy, J. A., J. S. Michaelson, and P. Leder. 2003. Homeodomain- interacting protein kinase 1 modulates Daxx localization, phosphorylation, and transcriptional activity. Mol. Cell. Biol. 23:950-960.
17. Eggenschwiler, J. T., E. Espinoza, and K. V. Anderson. 2001. Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature 412:194-198.
18. el-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
19. Engelhardt, O. G., C. Boutell, A. Orr, E. Ullrich, O. Haller, and R. D. Everett. 2003. The homeodomain-interacting kinase 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.
20. Epstein, D. J., M. Vekemans, and P. Gros. 1991. Splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3. Cell 67:767-774.
21. Fan, C. M., and M. Tessier-Lavigne. 1994. Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell 79:1175-1186.
22. Fan, C. M., J. A. Porter, C. Chiang, D. T. Chang, P. A. Beachy, and M. Tessier-Lavigne. 1995. Long-range sclerotome induction by sonic hedgehog: direct role of the amino-terminal cleavage product and modulation by the cyclic AMP signaling pathway. Cell 81:457-465.
23. Furumoto, T. A., N. Miura, T. Akasaka, Y. Mizutani-Koseki, H. Sudo, K. Fukuda, M. Maekawa, S. Yuasa, Y. Fu, H. Moriya, M. Taniguchi, K. Imai, E. Dahl, R. Balling, M. Pavlova, A. Gossler, and H. Koseki. 1999. Notochord-dependent expression of MFH1 and PAX1 cooperates to maintain the proliferation of sclerotome cells during the vertebral column development. Dev. Biol. 210:15-29.
24. Gondo, Y., K. Nakamura, K. Nakao, T. Sasaoka, K. Ito, M. Kimura, and M. Katsuki. 1994. Gene replacement of the p53 gene with the lacZ gene in mouse embryonic stem cells and mice by using two steps of homologous recombination. Biochem. Biophys. Res. Commun. 202:830-837.
25. Gresko, E., A. Moller, A. Roscic, and M. L. Schmitz. 2005. Covalent modification of human homeodomain interacting protein kinase 2 by SUMO-1 at lysine 25 affects its stability. Biochem. Biophys. Res. Commun. 329:1293-1299.
26. Harada, J., K. Kokura, C. Kanei-Ishii, T. Nomura, M. M. Khan, Y. Kim, and S. Ishii. 2003. Requirement of the co-repressor homeodomain-interacting protein kinase 2 for ski-mediated inhibition of bone morphogenetic protein-induced transcriptional activation. J. Biol. Chem. 278:38998-39005.
27. Harvey, M., A. T. Sands, R. S. Weiss, M. E. Hegi, R. W. Wiseman, P. Pantazis, B. C. Giovanella, M. A. Tainsky, A. Bradley, and L. A. Donehower. 1993. In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene 8:2457-2467.
28. Helwig, U., K. Imai, W. Schmahl, B. E. Thomas, D. S. Varnum, J. H. Nadeau, and R. Balling. 1995. Interaction between undulated and Patch leads to an extreme form of spina bifida in double-mutant mice. Nat. Genet. 11:60-63.
29. Herrera, E., E. Samper, and M. A. Blasco. 1999. Telomere shortening in mTR-/- embryos is associated with failure to close the neural tube. EMBO J. 18:1172-1181.
30. Hofmann, T. G., A. Moller, H. Sirma, H. Zentgraf, Y. Taya, W. Droge, H. Will, and M. L. Schmitz. 2002. Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nat. Cell Biol. 4:1-10.
31. 2- terminal kinase activation and apoptosis in human hepatoma cells. Cancer Res. 63:8271-8277.
32. Hofmann, T. G., E. Jaffray, N. Stollberg, R. T. Hay, and H. Will. 2005. Regulation of homeodomain-interacting protein kinase 2 (HIPK2) effector function through dynamic SUMO-1 modification. J. Biol. Chem. 280:29224-29232.
33. Hogan, B., R. Beddington, F. Costantini, and E. Lacy. 1994. Isolation, culture, and manipulation of embryonic stem cells, p. 253-290. In B. Hogan, F. Costantini, and E. Lacy (ed.), Manipulating the mouse embryo: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
34. Hollander, M. C., M. S. Sheikh, D. V. Bulavin, K. Lundgren, L. Augeri-Henmueller, R. Shehee, T. A. Molinaro, K. E. Kim, E. Tolosa, J. D. Ashwell, M. P. Rosenberg, Q. Zhan, P. M. Fernandez-Salguero, W. F. Morgan, C. X. Deng, and A. J. Fornace, Jr. 1999. Genomic instability in Gadd45a-deficient mice. Nat. Genet. 23:176-184.
35. Juriloff, D. M., and M. J. Harris. 2000. Mouse models for neural tube closure defects. Hum. Mol. Genet. 9:993-1000.
36. Kanei-Ishii, C., J. Ninomiya-Tsuji, J. Tanikawa, T. Nomura, T. Ishitani, S. Kishida, K. Kokura, T. Kurahashi, E. Ichikawa-Iwata, Y. Kim, K. Matsumoto, and S. Ishii. 2004. Wnt-1 signal induces phosphorylation and degradation of c-Myb protein via TAK1, HIPK2, and NLK. Genes Dev. 18:816-829.
37. Kim, Y. H., C. Y. Choi, S. J. Lee, M. A. Conti, and Y. Kim. 1998. Homeodomain-interacting protein kinases, a novel family of co-repressors for homeodomain transcription factors. J. Biol. Chem. 273:25875-25879.
38. Kim, Y. H., C. Y. Choi, and Y. Kim. 1999. Covalent modification of the homeodomain-interacting protein kinase 2 (HIPK2) by the ubiquitin-like protein SUMO-1. Proc. Natl. Acad. Sci. USA 96:12350-12355.
39. Kondo, S., Y. Lu, M. Debbas, A. W. Lin, I. Sarosi, A. Itie, A. Wakeham, J. Tuan, C. Saris, G. Elliott, W. Ma, S. Benchimol, S. W. Lowe, T. W. Mak, and S. K. Thukral. 2003. Characterization of cells and gene-targeted mice deficient for the p53-binding kinase homeodomain-interacting protein kinase 1 (HIPK1). Proc. Natl. Acad. Sci. USA 100:5431-5436.
40. Li, X., R. Zhang, D. Luo, S. J. Park, Q. Wang, Y. Kim, and W. Min. 2005. Tumor necrosis factor alpha-induced desumoylation and cytoplasmic translocation of homeodomain-interacting protein kinase 1 are critical for apoptosis signal-regulating kinase 1-JNK/p38 activation. J. Biol. Chem. 280:15061-15070.
41. Lohnes, D. 2003. The Cdx1 homeodomain protein: an integrator of posterior signaling in the mouse. Bioessays 25:971-980.
42. McMahon, J. A., S. Takada, L. B. Zimmerman, C. M. Fan, R. M. Harland, and A. P. McMahon. 1998. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12:1438-1452.
43. Miyashita, T., and J. C. Reed. 1995. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293-299.
44. Moilanen, A. M., U. Karvonen, H. Poukka, O. A. Janne, and J. J. Palvimo. 1998. Activation of androgen receptor function by a novel nuclear protein kinase. Mol. Biol. Cell 9:2527-2543.
45. Moller, A., H. Sirma, T. G. Hofmann, S. Rueffer, E. Klimczak, W. Droge, H. Will, and M. L. Schmitz. 2003. PML is required for homeodomain-interacting protein kinase 2 (HIPK2)-mediated p53 phosphorylation and cell cycle arrest but is dispensable for the formation of HIPK domains. Cancer Res. 63:4310-4314.
46. Moller, A., H. Sirma, T. G. Hofmann, H. Staege, E. Gresko, K. S. Ludi, E. Klimczak, W. Droge, H. Will, and M. L. Schmitz. 2003. Sp100 is important for the stimulatory effect of homeodomain-interacting protein kinase-2 on p53-dependent gene expression. Oncogene 22:8731-8737.
47. Oda, K., H. Arakawa, T. Tanaka, K. Matsuda, C. Tanikawa, T. Mori, H. Nishimori, K. Tamai, T. Tokino, Y. Nakamura, and Y. Taya. 2000. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102:849-862.
48. Packer, A. I., D. A. Crotty, V. A. Elwell, and D. J. Wolgemuth. 1998. Expression of the murine Hoxa4 gene requires both autoregulation and a conserved retinoic acid response element. Development 125:1991-1998.
49. Pani, L., M. Horal, and M. R. Loeken. 2002. Rescue of neural tube defects in Pax-3-deficient embryos by p53 loss of function: implications for Pax-3-dependent development and tumorigenesis. Genes Dev. 16:676-680.
50. Peters, H., B. Wilm, N. Sakai, K. Imai, R. Maas, and R. Balling. 1999. Pax1 and Pax9 synergistically regulate vertebral column development. Development 126:5399-5408.
51. Pierantoni, G. M., M. Fedele, F. Pentimalli, G. Benvenuto, R. Pero, G. Viglietto, M. Santoro, L. Chiariotti, and A. Fusco. 2001. High mobility group I (Y) proteins bind HIPK2, a serine-threonine kinase protein which inhibits cell growth. Oncogene 20:6132-6141.
52. Pierantoni, G. M., A. Bulfone, F. Pentimalli, M. Fedele, R. Iuliano, M. Santoro, L. Chiariotti, A. Ballabio, and A. Fusco. 2002. The homeodomain-interacting protein kinase 2 gene is expressed late in embryogenesis and preferentially in retina, muscle, and neural tissues. Biochem. Biophys. Res. Commun. 290:942-947.
53. Puri, P. L., K. Bhakta, L. D. Wood, A. Costanzo, J. Zhu, and J. Y. Wang. 2002. A myogenic differentiation checkpoint activated by genotoxic stress. Nat. Genet. 32:585-593.
54. Rastegar, M., L. Kobrossy, E. N. Kovacs, I. Rambaldi, and M. Featherstone. 2004. Sequential histone modifications at Hoxd4 regulatory regions distinguish anterior from posterior embryonic compartments. Mol. Cell. Biol. 24:8090-8103.
55. 2-terminal kinase activation. J. Exp. Med. 192:1165-1174.
56. Roelink, H., J. A. Porter, C. Cbiang, Y. Tanabe, D. T. Chang, P. A. Beachy, and T. M. Jessell. 1995. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of Sonic hedgehog autoproteolysis. Cell 81:445-455.
57. Rui, Y., Z. Xu, S. Lin, Q. Li, H. Rui, W. Luo, H. M. Zhou, P. Y. Cheung, Z. Wu, Z. Ye, P. Li, J. Han, and S. C. Lin. 2004. Axin stimulates p53 functions by activation of HIPK2 kinase through multimeric complex formation. EMBO J. 23:4583-4594.
58. Saga, Y., N. Hata, H. Koseki, and M. M. Taketo. 1997. Mesp2: a novel mouse gene expressed in the presegmented mesoderm and essential for segmentation initiation. Genes Dev. 11:1827-1839.
59. Sah, V. P., L. D. Attardi, G. J. Mulligan, B. O. Williams, R. T. Bronson, and T. Jacks. 1995. A subset of p53-deficient embryos exhibit exencephaly. Nat. Genet. 10:175-180.
60. Sung, K. S., Y. Y. Go, J. H. Ahn, Y. H. Kim, Y. Kim, and C. Y. Choi. 2005. Differential interactions of the homeodomain-interacting protein kinase 2 (HIPK2) by phosphorylation-dependent sumoylation. FEBS Lett. 579:3001-3008.
61. Takebayashi-Suzuki, K., J. Funami, D. Tokumori, A. Saito, T. Watabe, K. Miyazono, A. Kanda, and A. Suzuki. 2003. Interplay between the tumor suppressor p53 and TGF beta signaling shapes embryonic body axes in Xenopus. Development 130:3929-3939.
62. Wallin, J. W., H. Koseki, R. Fritsch, B. Christ, and R. Balling. 1994. The role of Pax1 in axial skeleton development. Development 120:1109-1121.
63. Wang, Y., E. M. Schneider, X. Li, I. Duttenhofer, K. Debatin, and H. Hug. 2002. HIPK2 associates with RanBPM. Biochem. Biophys. Res. Commun. 297:148-153.
64. Watanabe, K., T. Ozaki, T. Nakagawa, K. Miyazaki, M. Takahashi, M. Hosoda, S. Hayashi, S. Todo, and A. Nakagawara. 2002. Physical interaction of p73 with c-Myc and MM1, a c-Myc-binding protein, and modulation of the p73 function. J. Biol. Chem. 277:15113-15123.
65. Wiggins, A. K., G. Wei, E. Doxakis, C. Wong, A. A. Tang, K. Zang, E. J. Luo, R. L. Neve, L. F. Reichardt, and E. J. Huang. 2004. Interaction of Brn3a and H1PK2 mediates transcriptional repression of sensory neuron survival. J. Cell Biol. 167:257-267.
66. Ybot-Gonzalez, P., P. Cogram, D. Gerrelli, and A. J. Copp. 2002. Sonic hedgehog and the molecular regulation of mouse neural tube closure. Development 129:2507-2517.
67. Zakany, J., M. Kmita, P. Alarcon, J. L. de la Pompa, and D. Duboule. 2001. Localized and transient transcription of Hox genes suggests a link between patterning and the segmentation clock. Cell 106:207-217.
68. Zhang, Q., Y. Yoshimatsu, J. Hildebrand, S. M. Frisch, and R. H. Goodman. 2003. Homeodomain interacting protein kinase 2 promotes apoptosis by downregulating the transcriptional corepressor CtBP. Cell 115:177-186.
69. Zhang, Q., A. Nottke, and R. H. Goodman. 2005. Homeodomain-interacting protein kinase-2 mediates CtBP phosphorylation and degradation in UV-triggered apoptosis. Proc. Natl. Acad. Sci. USA 102:2802-2807.