Transcriptional regulation of ferritin and antioxidant genes by HIPK2 under genotoxic stress

Journal of Cell Science

Volumn 123, Issue 22, 2010, Pages 3863-3871

  Hailemariam, Kiros ^a,b   Iwasaki, Kenta ^a,c   Huang, Bo Wen ^a   Sakamoto, Kensuke ^a   Tsuji, Yoshiaki ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^c NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

ATF1; Ferritin; Genotoxic stress; HIPK2; Phosphorylation; Transcription

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 1; ARSENITE SODIUM; DOXORUBICIN; ETOPOSIDE; FERRITIN; FERRITIN H; GLUTATHIONE TRANSFERASE; HEME OXYGENASE 1; HOMEODOMAIN INTERACTING PROTEIN KINASE 2; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); UNCLASSIFIED DRUG;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELL STRAIN HEPG2; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; GENE EXPRESSION; GENOTOXICITY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION;

ACTIVATING TRANSCRIPTION FACTOR 1; CARRIER PROTEINS; CELL GROWTH PROCESSES; CELL SURVIVAL; DNA DAMAGE; FERRITINS; GENE EXPRESSION REGULATION; HUMANS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS;

EID: 78649726635     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.073627     Document Type: Article

References (68)

1. 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.
2. Arias, J., Alberts, A. S., Brindle, P., Claret, F. X., Smeal, T., Karin, M., Feramisco, J. and Montminy, M. (1994). Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature 370, 226-229.
3. Arosio, P. and Levi, S. (2002). Ferritin, iron homeostasis, and oxidative damage. Free Radic. Biol. Med. 33, 457-463.
4. Atlas, E., Stramwasser, M. and Mueller, C. R. (2001). A CREB site in the BRCA1 proximal promoter acts as a constitutive transcriptional element. Oncogene 20, 7110-7114.
5. Belmonte, N., Phillips, B. W., Massiera, F., Villageois, P., Wdziekonski, B., Saint-Marc, P., Nichols, J., Aubert, J., Saeki, K., Yuo, A. et al. (2001). Activation of extracellular signal-regulated kinases and CREB/ATF-1 mediate the expression of CCAAT/enhancer binding proteins beta and -delta in preadipocytes. Mol. Endocrinol. 15, 2037-2049.
6. Bosilevac, J. M., Olsen, R. J., Bridge, J. A. and Hinrichs, S. H. (1999). Tumor cell viability in clear cell sarcoma requires DNA binding activity of the EWS/ATF1 fusion protein. J. Biol. Chem. 274, 34811-34818.
7. Boucher, M. J., Simoneau, M. and Edlund, H. (2009). The homeodomain-interacting protein kinase 2 regulates insulin promoter factor-1/pancreatic duodenal homeobox-1 transcriptional activity. Endocrinology 150, 87-97.
8. Calzado, M. A., Renner, F., Roscic, A. and Schmitz, M. L. (2007). HIPK2: a versatile switchboard regulating the transcription machinery and cell death. Cell Cycle 6, 139-143.
9. Calzado, M. A., de la Vega, L., Moller, A., Bowtell, D. D. and Schmitz, M. L. (2009a). An inducible autoregulatory loop between HIPK2 and Siah2 at the apex of the hypoxic response. Nat. Cell Biol. 11, 85-91.
10. Calzado, M. A., De la Vega, L., Munoz, E. and Schmitz, M. L. (2009b). From top to bottom: the two faces of HIPK2 for regulation of the hypoxic response. Cell Cycle 8, 1659-1664.
11. 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, 21427-21436.
12. Choi, D. W., Seo, Y. M., Kim, E. A., Sung, K. S., Ahn, J. W., Park, S. J., Lee, S. R. and Choi, C. Y. (2008). Ubiquitination and degradation of homeodomain-interacting protein kinase 2 by WD40 repeat/SOCS box protein WSB-1. J. Biol. Chem. 283, 4682-4689.
13. Chrivia, J. C., Kwok, R. P. S., Lamb, N., Hagiwara, M., Montominy, M. R. and Goodman, R. H. (1993). Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365, 855-859.
14. Dong, Y., Asch, H. L., Ying, A. and Asch, B. B. (2002). Molecular mechanism of transcriptional repression of gelsolin in human breast cancer cells. Exp. Cell Res. 276, 328-336.
15. D'Orazi, G., Cecchinelli, B., Bruno, T., Manni, I., Higashimoto, Y., Saito, S., Gostissa, M., Coen, S., Marchetti, A., Del Sal, G. et al. (2002). Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat. Cell Biol. 4, 11-19.
16. Ebert, B. L. and Bunn, H. F. (1998). Regulation of transcription by hypoxia requires a multiprotein complex that includes hypoxia-inducible factor 1, an adjacent transcription factor, and p300/CREB binding protein. Mol. Cell. Biol. 18, 4089-4096.
17. Hentze, M. W., Muckenthaler, M. U. and Andrews, N. C. (2004). Balancing acts: molecular control of mammalian iron metabolism. Cell 117, 285-297.
18. Hofmann, T. G., Mincheva, A., Lichter, P., Droge, W. and Schmitz, M. L. (2000). Human homeodomain-interacting protein kinase-2 (HIPK2) is a member of the DYRK family of protein kinases and maps to chromosome 7q32-q34. Biochimie 82, 1123-1127.
19. Hofmann, T. G., Moller, A., Sirma, H., Zentgraf, H., Taya, Y., Droge, 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.
20. Hsueh, Y. P. and Lai, M. Z. (1995). Overexpression of activation transcriptional factor 1 in lymphomas and in activated lymphocytes. J. Immunol. 154, 5675-5683.
21. Iwasaki, K., Mackenzie, E. L., Hailemariam, K., Sakamoto, K. and Tsuji, Y. (2006). Hemin-mediated regulation of an antioxidant-responsive element of the human ferritin H gene and role of Ref-1 during erythroid differentiation of K562 cells. Mol. Cell. Biol. 26, 2845-2856.
22. Iwasaki, K., Hailemariam, K. and Tsuji, Y. (2007). PIAS3 interacts with ATF1 and regulates the human ferritin H gene through an antioxidant-responsive element. J. Biol. Chem. 282, 22335-22343.
23. Jean, D., Tellez, C., Huang, S., Davis, D. W., Bruns, C. J., McConkey, D. J., Hinrichs, S. H. and Bar-Eli, M. (2000). Inhibition of tumor growth and metastasis of human melanoma by intracellular anti-ATF-1 single chain Fv fragment. Oncogene 19, 2721-2730.
24. Kakhlon, O., Gruenbaum, Y. and Cabantchik, Z. I. (2001). Repression of the heavy ferritin chain increases the labile iron pool of human K562 cells. Biochem. J. 356, 311-316.
25. Kaur, D., Yantiri, F., Rajagopalan, S., Kumar, J., Mo, J. Q., Boonplueang, R., Viswanath, V., Jacobs, R., Yang, L., Beal, M. F. et al. (2003). Genetic or pharmacological iron chelation prevents MPTP-induced neurotoxicity in vivo: a novel therapy for Parkinson's disease. Neuron 37, 899-909.
26. Kim, Y. H., Choi, C. Y., Lee, S. J., Conti, M. A. and Kim, Y. (1998). Homeodomain-interacting protein kinases, a novel family of co-repressors for homeodomain transcription factors. J. Biol. Chem. 273, 25875-25879.
27. Kingsley-Kallesen, M. L., Kelly, D. and Rizzino, A. (1999). Transcriptional regulation of the transforming growth factor-beta2 promoter by cAMP-responsive element-binding protein (CREB) and activating transcription factor-1 (ATF-1) is modulated by protein kinases and the coactivators p300 and CREB-binding protein. J. Biol. Chem. 274, 34020-34028.
28. Kvietikova, I., Wenger, R. H., Marti, H. H. and Gassmann, M. (1995). The transcription factors ATF-1 and CREB-1 bind constitutively to the hypoxia-inducible factor-1 (HIF-1) DNA recognition site. Nucleic Acids Res. 23, 4542-4550.
29. Kwok, R. P. S., Lundblad, J. R., Chrivia, J. C., Richards, J. P., Bachinger, H. P., Brennan, R. G., Roberts, S. G. E., Green, M. R. and Goodman, R. H. (1994). Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370, 223-226.
30. Lee, M. G. and Pedersen, P. L. (2003). Glucose metabolism in cancer: importance of transcription factor-DNA interactions within a short segment of the proximal region of the type II hexokinase promoter. J. Biol. Chem. 278, 41047-41058.
31. Lu, Z. and Sack, M. N. (2008). ATF-1 is a hypoxia-responsive transcriptional activator of skeletal muscle mitochondrial-uncoupling protein 3. J. Biol. Chem. 283, 23410-23418.
32. MacKenzie, E. L. and Tsuji, Y. (2008). Elevated intracellular calcium increases ferritin H expression through an NFAT-independent post-transcriptional mechanism involving mRNA stabilization. Biochem. J. 411, 107-113.
33. MacKenzie, E. L., Iwasaki, K. and Tsuji, Y. (2008a). Intracellular iron transport and storage: from molecular mechanisms to health implications. Antioxid. Redox. Signal. 10, 997-1030.
34. MacKenzie, E. L., Ray, P. D. and Tsuji, Y. (2008b). Role and regulation of ferritin H in rotenone-mediated mitochondrial oxidative stress. Free Radic. Biol. Med. 44, 1762-1771.
35. Mayr, B. and Montminy, M. (2001). Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609.
36. Motohashi, H. and Yamamoto, M. (2004). Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol. Med. 10, 549-557.
37. Nardinocchi, L., Puca, R., Sacchi, A. and D'Orazi, G. (2009). Inhibition of HIF-1alpha activity by homeodomain-interacting protein kinase-2 correlates with sensitization of chemoresistant cells to undergo apoptosis. Mol. Cancer 8, 1.
38. Okuyama, Y., Sowa, Y., Fujita, T., Mizuno, T., Nomura, H., Nikaido, T., Endo, T. and Sakai, T. (1996). ATF site of human RB gene promoter is a responsive element of myogenic differentiation. FEBS Lett. 397, 219-224.
39. Papanikolaou, G. and Pantopoulos, K. (2005). Iron metabolism and toxicity. Toxicol. Appl. Pharmacol. 202, 199-211.
40. Pham, C. G., Bubici, C., Zazzeroni, F., Papa, S., Jones, J., Alvarez, K., Jayawardena, S., De Smaele, E., Cong, R., Beaumont, C. et al. (2004). Ferritin heavy chain upregulation by NF-kappaB inhibits TNFalpha-induced apoptosis by suppressing reactive oxygen species. Cell 119, 529-542.
41. Rehfuss, R. P., Walton, K. M., Loriaux, M. M. and Goodman, R. H. (1991). The cAMP-regulated enhancer-binding protein ATF-1 activates transcription in response to cAMP-dependent protein kinase A. J. Biol. Chem. 266, 18431-18434.
42. Rinaldo, C., Prodosmo, A., Siepi, F. and Soddu, S. (2007). HIPK2: a multitalented partner for transcription factors in DNA damage response and development. Biochem. Cell Biol. 85, 411-418.
43. Rolli, M., Kotlyarov, A., Sakamoto, K. M., Gaestel, M. and Neininger, A. (1999). Stress-induced stimulation of early growth response gene-1 by p38/stress-activated protein kinase 2 is mediated by a cAMP-responsive promoter element in a MAPKAP kinase 2-independent manner. J. Biol. Chem. 274, 19559-19564.
44. Rouault, T. A. (2006). The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2, 406-414.
45. Sakamoto, K., Iwasaki, K., Sugiyama, H. and Tsuji, Y. (2009). Role of the tumor suppressor PTEN in antioxidant responsive element-mediated transcription and associated histone modifications. Mol. Biol. Cell 20, 1606-1617.
46. Sakamoto, K., Huang, B. W., Iwasaki, K., Hailemariam, K., Ninomiya-Tsuji, J. and Tsuji, Y. (2010). Regulation of genotoxic stress response by homeodomain-interacting protein kinase 2 through phosphorylation of cyclic AMP response element-binding protein at serine 271. Mol. Biol. Cell 21, 2966-2974.
47. Salnikow, K., Wang, S. and Costa, M. (1997). Induction of activating transcription factor 1 by nickel and its role as a negative regulator of thrombospondin I gene expression. Cancer Res. 57, 5060-5066.
48. Shaywitz, A. J. and Greenberg, M. E. (1999). CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68, 821-861.
49. Sombroek, D. and Hofmann, T. G. (2009). How cells switch HIPK2 on and off. Cell Death Differ. 16, 187-194.
50. Theil, E. C. (2003). Ferritin: at the crossroads of iron and oxygen metabolism. J. Nutr. 133, 1549S-1553S.
51. Tsuji, Y. (2005). JunD activates transcription of the human ferritin H gene through an antioxidant response element during oxidative stress. Oncogene 24, 7567-7578.
52. Tsuji, Y., Kwak, E., Saika, T., Torti, S. V. and Torti, F. M. (1993a). Preferential repression of the H subunit of ferritin by adenovirus E1A in NIH-3T3 mouse fibroblasts. J. Biol. Chem. 268, 7270-7275.
53. Tsuji, Y., Ninomiya-Tsuji, J., Torti, S. V. and Torti, F. M. (1993b). Augmentation by IL-1a of tumor necrosis factor-a cytotoxicity in cells transfected with adenovirus E1A. J. Immunol. 150, 1897-1907.
54. Tsuji, Y., Akebi, N., Lam, T. K., Nakabeppu, Y., Torti, S. V. and Torti, F. M. (1995). FER-1, an enhancer of the ferritin H gene and a target of E1A-mediated transcriptional repression. Mol. Cell. Biol. 15, 5152-5164.
55. Tsuji, Y., Ayaki, H., Whitman, S. P., Morrow, C. S., Torti, S. V. and Torti, F. M. (2000). Coordinate transcriptional and translational regulation of ferritin in response to oxidative stress. Mol. Cell. Biol. 20, 5818-5827.
56. Wang, Y., Hofmann, T. G., Runkel, L., Haaf, T., Schaller, H., Debatin, K. and Hug, H. (2001). Isolation and characterization of cDNAs for the protein kinase HIPK2. Biochim. Biophys. Acta 1518, 168-172.
57. Wasserman, W. W. and Fahl, W. E. (1997). Functional antioxidant responsive elements. Proc. Natl. Acad. Sci. USA 94, 5361-5366.
58. Wei, G., Ku, S., Ma, G. K., Saito, S., Tang, A. A., Zhang, J., Mao, J. H., Appella, E., Balmain, A. and Huang, E. J. (2007). HIPK2 represses beta-catenin-mediated transcription, epidermal stem cell expansion, and skin tumorigenesis. Proc. Natl. Acad. Sci. USA 104, 13040-13045.
59. Wiggin, G. R., Soloaga, A., Foster, J. M., Murray-Tait, V., Cohen, P. and Arthur, J. S. (2002). MSK1 and MSK2 are required for the mitogen- and stress-induced phosphorylation of CREB and ATF1 in fibroblasts. Mol. Cell. Biol. 22, 2871-2881.
60. Wiggins, A. K., Wei, G., Doxakis, E., Wong, C., Tang, A. A., Zang, K., Luo, E. J., Neve, R. L., Reichardt, L. F. and Huang, E. J. (2004). Interaction of Brn3a and HIPK2 mediates transcriptional repression of sensory neuron survival. J. Cell Biol. 167, 257-267.
61. Winter, M., Sombroek, D., Dauth, I., Moehlenbrink, J., Scheuermann, K., Crone, J. and Hofmann, T. G. (2008). Control of HIPK2 stability by ubiquitin ligase Siah-1 and checkpoint kinases ATM and ATR. Nat. Cell. Biol. 10, 812-824.
62. Wu, K. J., Polack, A. and Dalla-Favera, R. (1999). Coordinated regulation of iron-controlling genes, H-ferritin and IRP2, by c-MYC. Science 283, 676-679.
63. Zaman, K., Ryu, H., Hall, D., O'Donovan, K., Lin, K. I., Miller, M. P., Marquis, J. C., Baraban, J. M., Semenza, G. L. and Ratan, R. R. (1999). Protection from oxidative stress-induced apoptosis in cortical neuronal cultures by iron chelators is associated with enhanced DNA binding of hypoxia-inducible factor-1 and ATF-1/CREB and increased expression of glycolytic enzymes, p21(waf1/cip1), and erythropoietin. J. Neurosci. 19, 9821-9830.
64. Zhang, J., Pho, V., Bonasera, S. J., Holtzman, J., Tang, A. T., Hellmuth, J., Tang, S., Janak, P. H., Tecott, L. H. and Huang, E. J. (2007). Essential function of HIPK2 in TGFbeta-dependent survival of midbrain dopamine neurons. Nat. Neurosci. 10, 77-86.
65. Zhang, J. W., Klemm, D. J., Vinson, C. and Lane, M. D. (2004). Role of CREB in transcriptional regulation of CCAAT/enhancer-binding protein beta gene during adipogenesis. J. Biol. Chem. 279, 4471-4478.
66. Zhang, Q., Yoshimatsu, Y., Hildebrand, J., Frisch, S. M. and Goodman, R. H. (2003). Homeodomain interacting protein kinase 2 promotes apoptosis by downregulating the transcriptional corepressor CtBP. Cell 115, 177-186.
67. Zhang, Q., Nottke, A. and Goodman, R. H. (2005). Homeodomain-interacting protein kinase-2 mediates CtBP phosphorylation and degradation in UV-triggered apoptosis. Proc. Natl. Acad. Sci. USA 102, 2802-2807.
68. Zucman, J., Delattre, O., Desmaze, C., Epstein, A. L., Stenman, G., Speleman, F., Fletchers, C. D., Aurias, A. and Thomas, G. (1993). EWS and ATF-1 gene fusion induced by t(12;22) translocation in malignant melanoma of soft parts. Nat. Genet. 4, 341-345.