The ING4 tumor suppressor attenuates NF-κB activity at the promoters of target genes

Molecular and Cellular Biology

Volumn 28, Issue 21, 2008, Pages 6632-6645

  Nozell, Susan ^a   Laver, Travis ^a   Moseley, Dorothy ^a   Nowoslawski, Lisa ^a   DeVos, Marijke ^a   Atkinson, George P ^a   Harrison, Keith ^b   Nabors, L Burton ^c   Benveniste, Etty N ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c The University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; GELATINASE B; HISTONE DEACETYLASE 1; HISTONE H3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF GROWTH 4 PROTEIN; PROTEIN P300; SYNAPTOTAGMIN I; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; E1A ASSOCIATED P300 PROTEIN; EP300 PROTEIN, HUMAN; HDAC1 PROTEIN, HUMAN; HISTONE; HISTONE DEACETYLASE; HOMEODOMAIN PROTEIN; ING4 PROTEIN, HUMAN; PTGS2 PROTEIN, HUMAN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RELA;

ACETYLATION; ARTICLE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; DNA BINDING; GENE EXPRESSION REGULATION; GENE TARGETING; GLIOMA; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; CELL NUCLEUS; DOSE RESPONSE; DRUG EFFECT; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROTEIN TRANSPORT; TUMOR CELL LINE; TUMOR GENE;

CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL NUCLEUS; CYCLOOXYGENASE 2; DOSE-RESPONSE RELATIONSHIP, DRUG; E1A-ASSOCIATED P300 PROTEIN; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, NEOPLASM; GLIOMA; HISTONE DEACETYLASES; HISTONES; HOMEODOMAIN PROTEINS; HUMANS; MATRIX METALLOPROTEINASE 9; NF-KAPPA B; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 55449102824     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00697-08     Document Type: Article

References (45)

1. Barboric, M., R. M. Nissen, S. Kanazawa, N. Jabrane-Ferrat, and B. M. Peterlin. 2001. NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol. Cell 8:327-337.
2. Bernstein, B. E., M. Kamal, K. Lindblad-Toh, S. Bekiranov, D. K. Bailey, D. J. Huebert, S. McMahon, E. K. Karlsson, E. J. Kulbokas III, T. R. Gingeras, S. L. Schreiber, and E. S. Lander. 2005. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120:169-181.
3. Buccoliero, A. M., A. Caldarella, C. F. Gheri, A. Taddei, M. Paglierani, M. Pepi, P. Mennonna, and G. L. Taddei. 2006. Inducible cyclooxygenase (COX-2) in glioblastoma: clinical and immunohistochemical (COX-2-VEGF) correlations. Clin. Neuropathol. 25:59-66.
4. Campos, E. I., M. Y. Chin, W. H. Kuo, and G. Li. 2004. Biological functions of the ING family tumor suppressors. Cell. Mol. Life Sci. 61:2597-2613.
5. Choi, C., O. Kutsch, J. Park, T. Zhou, D. W. Seol, and E. N. Benveniste. 2002. Tumor necrosis factor-related apoptosis-inducing ligand induces caspase-dependent interleukin-8 expression and apoptosis in human astroglioma cells. Mol. Cell. Biol. 22:724-736.
6. Doyon, Y., C. Cayrou, M. Ullah, A. J. Landry, V. Cote, W. Selleck, W. S. Lane, S. Tan, X. J. Yang, and J. Cote. 2006. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol. Cell 21:51-64.
7. Furnari, F. B., T. Fenton, R. M. Bachoo, A. Mukasa, J. M. Stommel, A. Stegh, W. C. Hahn, K. L. Ligon, D. N. Louis, C. Brennan, L. Chin, R. A. DePinho, and W. K. Cavenee. 2007. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 21:2683-2710.
8. Garkavtsev, I., S. V. Kozin, O. Chernova, L. Xu, F. Winkler, E. Brown, G. H. Barnett, and R. K. Jain. 2004. The candidate tumour suppressor protein ING4 regulates brain tumour growth and angiogenesis. Nature 428:328-332.
9. Gong, W., K. Suzuki, M. Russell, and K. Riabowol. 2005. Function of the ING family of PHD proteins in cancer. Int. J. Biochem. Cell Biol. 37:1054-1065.
10. Gunduz, M., H. Nagatsuka, K. Demircan, E. Gunduz, B. Cengiz, M. Ouchida, H. Tsujigiwa, E. Yamachika, K. Fukushima, L. Beder, S. Hirohata, Y. Ninomiya, K. Nishizaki, K. Shimizu, and N. Nagai. 2005. Frequent deletion and down-regulation of ING4, a candidate tumor suppressor gene at 12p13, in head and neck squamous cell carcinomas. Gene 356:109-117.
11. He, C. 1996. Molecular mechanism of transcriptional activation of human gelatinase B by proximal promoter. Cancer Lett. 106:185-191.
12. He, G. H., C. C. Helbing, M. J. Wagner, C. W. Sensen, and K. Riabowol. 2005. Phylogenetic analysis of the ING family of PHD finger proteins. Mol. Biol. Evol. 22:104-116.
13. Hoffmann, A., G. Natoli, and G. Ghosh. 2006. Transcriptional regulation via the NF-κB signaling module. Oncogene 25:6706-6716.
14. Karin, M., Y. Cao, F. R. Greten, and Z. W. Li. 2002. NF-êB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer. 2:301-310.
15. Kim, S., K. Chin, J. W. Gray, and J. M. Bishop. 2004. A screen for genes that suppress loss of contact inhibition: identification of ING4 as a candidate tumor suppressor gene in human cancer. Proc. Natl. Acad. Sci. USA 101:16251-16256.
16. Lakka, S. S., S. L. Jasti, C. Gondi, D. Boyd, N. Chandrasekar, D. H. Dinh, W. C. Olivero, M. Gujrati, and J. S. Rao. 2002. Downregulation of MMP-9 in ERK-mutated stable transfectants inhibits glioma invasion in vitro. Oncogene 21:5601-5608.
17. Ma, Z., M. J. Chang, R. C. Shah, and E. N. Benveniste. 2005. Interferon-gamma-activated STAT-1alpha suppresses MMP-9 gene transcription by sequestration of the coactivators CBP/p300. J. Leukoc. Biol. 78:515-523.
18. Ma, Z., H. Qin, and E. N. Benveniste. 2001. Transcriptional suppression of matrix metalloproteinase-9 gene expression by IFN-gamma and IFN-beta: critical role of STAT-1alpha. J. Immunol. 167:5150-5159.
19. Ma, Z., R. C. Shah, M. J. Chang, and E. N. Benveniste. 2004. Coordination of cell signaling, chromatin remodeling, histone modifications, and regulator recruitment in human matrix metalloproteinase 9 gene transcription. Mol. Cell. Biol. 24:5496-5509.
20. Maher, E. A., F. B. Furnari, R. M. Bachoo, D. H. Rowitch, D. N. Louis, W. K. Cavenee, and R. A. DePinho. 2001. Malignant glioma: genetics and biology of a grave matter. Genes Dev. 15:1311-1333.
21. Marshall, R. M., and X. Grana. 2006. Mechanisms controlling CDK9 activity. Front. Biosci. 11:2598-2613.
22. Martin, D. G., K. Baetz, X. Shi, K. L. Walter, V. E. MacDonald, M. J. Wlodarski, O. Gozani, P. Hieter, and L. Howe. 2006. The Yng1p plant homeodomain finger is a methyl-histone binding module that recognizes lysine 4-methylated histone H3. Mol. Cell. Biol. 26:7871-7879.
23. Ng, H. H., F. Robert, R. A. Young, and K. Struhl. 2003. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11:709-719.
24. Nowoslawski, L., B. J. Klocke, and K. A. Roth. 2005. Molecular regulation of acute ethanol-induced neuron apoptosis. J. Neuropathol. Exp. Neurol. 64:490-497.
25. Nozell, S., T. Laver, K. Patel, and E. N. Benveniste. 2006. Mechanism of IFN-beta-mediated inhibition of IL-8 gene expression in astroglioma cells. J. Immunol. 177:822-830.
26. Nozell, S., Z. Ma, C. Wilson, R. Shah, and E. N. Benveniste. 2004. Class II major histocompatibility complex transactivator (CIITA) inhibits matrix metalloproteinase-9 gene expression. J. Biol. Chem. 279:38577- 38589.
27. Ozer, A., and R. K. Bruick. 2005. Regulation of HIF by prolyl hydroxylases: recruitment of the candidate tumor suppressor protein ING4. Cell Cycle 4:1153-1156.
28. Ozer, A., L. C. Wu, and R. K. Bruick. 2005. The candidate tumor suppressor ING4 represses activation of the hypoxia inducible factor (HIF). Proc. Natl. Acad. Sci. USA 102:7481-7486.
29. Palacios, A., P. Garcia, D. Padro, E. Lopez-Hernandez, I. Martin, and F. J. Blanco. 2006. Solution structure and NMR characterization of the binding to methylated histone tails of the plant homeodomain finger of the tumour suppressor ING4. FEBS Lett. 580:6903-6908.
30. Pena, P. V., F. Davrazou, X. Shi, K. L. Walter, V. V. Verkhusha, O. Gozani, R. Zhao, and T. G. Kutateladze. 2006. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 442:100-103.
31. Peterlin, B. M., and D. H. Price. 2006. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23:297-305.
32. Phatnani, H. P., and A. L. Greenleaf. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20:2922-2936.
33. Santos-Rosa, H., and C. Caldas. 2005. Chromatin modifier enzymes, the histone code and cancer. Eur. J. Cancer 41:2381-2402.
34. Santos-Rosa, H., R. Schneider, A. J. Bannister, J. Sherriff, B. E. Bernstein, N. C. Emre, S. L. Schreiber, J. Mellor, and T. Kouzarides. 2002. Active genes are tri-methylated at K4 of histone H3. Nature 419:407-411.
35. Schmedtje, J. F., Jr., Y. S. Ji, W. L. Liu, R. N. DuBois, and M. S. Runge. 1997. Hypoxia induces cyclooxygenase-2 via the NF-κB p65 transcription factor in human vascular endothelial cells. J. Biol. Chem. 272:601-608.
36. Schneider, R., A. J. Bannister, F. A. Myers, A. W. Thorne, C. Crane-Robinson, and T. Kouzarides. 2004. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat. Cell Biol. 6:73-77.
37. Shi, X., T. Hong, K. L. Walter, M. Ewalt, E. Michishita, T. Hung, D. Carney, P. Pena, F. Lan, M. R. Kaadige, N. Lacoste, C. Cayrou, F. Davrazou, A. Saha, B. R. Cairns, D. E. Ayer, T. G. Kutateladze, Y. Shi, J. Cote, K. F. Chua, and O. Gozani. 2006. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442:96-99.
38. Shiseki, M., M. Nagashima, R. M. Pedeux, M. Kitahama-Shiseki, K. Miura, S. Okamura, H. Onogi, Y. Higashimoto, E. Appella, J. Yokota, and C. C. Harris. 2003. p29ING4 and p28ING5 bind to p53 and p300, and enhance p53 activity. Cancer Res. 63:2373-2378.
39. Taverna, S. D., S. Ilin, R. S. Rogers, J. C. Tanny, H. Lavender, H. Li, L. Baker, J. Boyle, L. P. Blair, B. T. Chait, D. J. Patel, J. D. Aitchison, A. J. Tackett, and C. D. Allis. 2006. Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol. Cell 24:785-796.
40. Unoki, M., J. C. Shen, Z. M. Zheng, and C. C. Harris. 2006. Novel splice variants of ING4 and their possible roles in the regulation of cell growth and motility. J. Biol. Chem. 281:34677-34686.
41. Van den Steen, P. E., B. Dubois, I. Nelissen, P. M. Rudd, R. A. Dwek, and G. Opdenakker. 2002. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit. Rev. Biochem. Mol. Biol. 37:375-536.
42. Wang, H., H. Wang, W. Zhang, H. J. Huang, W. S. Liao, and G. N. Fuller. 2004. Analysis of the activation status of Akt, NF-κB, and Stat3 in human diffuse gliomas. Lab. Investig. 84:941-951.
43. Zhang, X., K. S. Wang, Z. Q. Wang, L. S. Xu, Q. W. Wang, F. Chen, D. Z. Wei, and Z. G. Han. 2005. Nuclear localization signal of ING4 plays a key role in its binding to p53. Biochem. Biophys. Res. Commun. 331:1032- 1038.
44. Zhong, H., M. J. May, E. Jimi, and S. Ghosh. 2002. The phosphorylation status of nuclear NF-êB determines its association with CBP/p300 or HDAC-1. Mol. Cell 9:625-636.
45. Zhong, H., R. E. Voll, and S. Ghosh. 1998. Phosphorylation of NF-êB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell 1:661-671.