The novel Nrf2-interacting factor KAP1 regulates susceptibility to oxidative stress by promoting the Nrf2-mediated cytoprotective response

Biochemical Journal

Volumn 436, Issue 2, 2011, Pages 387-397

  Maruyama, Atsushi ^a   Nishikawa, Keizo ^b   Kawatani, Yukie ^c   Mimura, Junsei ^a   Hosoya, Tomonori ^a   Harada, Nobuhiko ^a   Yamamato, Masayuki ^c   Itoh, Ken ^a  

^a HIROSAKI UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Haem oxygenase 1 (HO 1); Kr ppel associated box associated protein 1 (KAP1); NAD(P)H quinone oxido reductase 1 (NQO1); Nuclear factor erythroid 2 related factor 2 (Nrf2); Oxidative stress; Transcription regulation

Indexed keywords

DIAMIDE; HEME OXYGENASE 1; HYDROGEN PEROXIDE; KRUPPEL ASSOCIATED BOX ASSOCIATED PROTEIN 1; MALEIC ACID DIETHYL ESTER; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REGULATOR PROTEIN; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL PROTECTION; CELL STRAIN 3T3; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENHANCER REGION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; TRANSACTIVATION;

ANIMALS; CELLS, CULTURED; CYTOPROTECTION; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; NIH 3T3 CELLS; OXIDATIVE STRESS; PROTEIN BINDING; REPRESSOR PROTEINS;

EID: 79956042344     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20101748     Document Type: Article

References (45)

1. Itoh, K., Tong, K. I. and Yamamoto, M. (2004) Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radical Biol. Med. 36, 1208-1213
2. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J. D. and Yamamoto, M. (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13, 76-86 (Pubitemid 29045117)
3. Kobayashi, A., Kang, M. I., Okawa, H., Ohtsuji, M., Zenke, Y., Chiba, T., Igarashi, K. and Yamamoto, M. (2004) Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24, 7130-7139
4. Zhang, D. D. and Hannink, M. (2003) Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol. Cell. Biol. 22, 8137-8151
5. Motohashi, H., Katsuoka, F., Engel, J. D. and Yamamoto, M. (2004) Small Maf proteins serve as transcriptional cofactors for keratinocyte differentiation in the Keap1-Nrf2 regulatory pathway. Proc. Natl. Acad. Sci. U.S.A. 101, 6379-6384
6. Chan, K. and Kan, Y. W. (1999) Nrf2 is essential for protection against acute pulmonary injury in mice. Proc. Natl. Acad. Sci. U.S.A. 96, 12731-12736
7. Ramos-Gomez, M., Kwak, M. K., Dolan, P. M., Itoh, K., Yamamoto, M., Talalay, P. and Kensler, T. W. (2001) Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 98, 3410-3415
8. 2. Mol. Cell. Biol. 24, 36-45
9. Li, J., Stein, T. D. and Johnson, J. A. (2004) Genetic dissection of systemic autoimmune disease in Nrf2-deficient mice. Physiol. Genomics 18, 261-272
10. Khetchoumian, K., Teletin, M., Mark, M., Lerouge, T., Cerviño, M., Oulad-Abdelghani, M., Chambon, P. and Losson, R. (2004) TIF1δ, a novel HP1-interacting member of the transcriptional intermediary factor 1 (TIF1) family expressed by elongating spermatids. J. Biol. Chem. 279, 48329-48341
11. Ozato, K., Shin, D.-M., Chang, T. H. and Morse, III, H. C. (2008) TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 8, 849-860
12. Peng, H., Feldman, I. and Rauscher, III, F. J. (2002) Hetero-oligomerization among the TIF family of RBCC/TRIM domain-containing nuclear cofactors: a potential mechanism for regulating the switch between coactivation and corepression. J. Mol. Biol. 320, 629-644
13. Huntley, S., Baggott, D. M., Hamilton, A. T., Tran-Gyamfi, M., Yang, S., Kim, J., Gordon, L., Branscomb, E. and Stubbs, L. (2006) A comprehensive catalog of human KRAB-associated zinc finger genes: insights into the evolutionary history of a large family of transcriptional repressors. Genome Res. 16, 669-677
14. Ayyanathan, K., Lechner, M. S., Bell, P., Maul, G. G., Schultz, D. C., Yamada, Y., Tanaka, K., Torigoe, K. and Rauscher, III, F. J. (2003) Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: a mammalian cell culture model of gene variegation. Genes Dev. 17, 1855-1869 (Pubitemid 36944563)
15. Le Douarin, B., Nielsen, A. L., Garnier, J.-M., Ishinose, H., Jeanmougin, F., Losson, R. and Chambon, P. (1996) A possible involvement of TIF1α and TIF1β in the epigenetic control of transcription by nuclear receptors. EMBO J. 15, 6701-6715 (Pubitemid 26413802)
16. Schultz, D. C., Friedman, J. R. and Rauscher, III, F. J. (2001) Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2α subunit of NuRD. Genes Dev. 15, 428-443 (Pubitemid 32187004)
17. Schultz, D. C., Ayyanathan, K., Negorev, D., Maul, G. G. and Rauscher, III, F. J. (2002) SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 16, 919-932 (Pubitemid 34408542)
18. Sripathy, S. P., Stevens, J. and Schultz, D. C. (2006) The KAP1 corepressor functions to coordinate the assembly of de novo HP1-demarcated microenvironments of heterochromatin required for KRAB zinc finger protein-mediated transcriptional repression. Mol. Cell. Biol. 26, 8623-8638
19. Ivanov, A. V., Peng, H., Yurchenko, V., Yap, K. L., Negorev, D. G., Schultz, D. C., Psulkowski, E., Fredericks, W. J., White, D. E., Maul, G. G. et al. (2008) PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol. Cell 28, 823-837 (Pubitemid 350217061)
20. Chang, C.-J., Chen, Y.-L. and Lee, S.-C. (1998) Coactivator TIF1β interacts with transcription factor C/EBPβ and glucocorticoid receptor to induce α1-acid glycoprotein gene expression. Mol. Cell. Biol. 18, 5880-5887
21. Rambaud, J., Desroches, J., Balsalobre, A. and Drouin, J. (2009) TIF1β/KAP-1 is a coactivator of the orphan nuclear receptor NGFI-B/Nur77. J. Biol. Chem. 284, 14147-14156
22. Katoh, Y., Itoh, K., Yoshida, E., Miyagishi, M., Fukamizu, A. and Yamamoto, M. (2001) Two domains of Nrf2 cooperatively bind CBP, a CREB binding protein, and synergistically activate transcription. Genes Cells 6, 857-868 (Pubitemid 33019739)
23. Zhang, J., Ohta, T., Maruyama, A., Hosoya, T., Nishikawa, K., Maher, J. M., Shibahara, S., Itoh, K. and Yamamoto, M. (2006) BRG1 interacts with Nrf2 to selectively mediate HO-1 induction in response to oxidative stress. Mol. Cell. Biol. 26, 7942-7952
24. Zhang, J., Hosoya, T., Maruyama, A., Nishikawa, K., Maher, J. M., Ohta, T., Motohashi, H., Fukamizu, A., Shibahara, S., Itoh, K. and Yamamoto, M. (2007) Nrf2 Neh5 domain is differentially utilized in the transactivation of cytoprotective genes. Biochem. J. 404, 459-466 (Pubitemid 46953920)
25. Nioi, P., Nguyen, T., Sherratt, P. J. and Pickett, C. B. (2005) The carboxy-terminal Neh3 domain of Nrf2 is required for transcriptional activation. Mol. Cell. Biol. 25, 10895-10906
26. Dignam, J. D., Lebovitz, R. M. and Roeder, R. G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489
27. Tsuruma, R., Ohbayashi, N., Kamitani, S., Ikeda, O., Sato, N., Muromoto, R, Sekine, Y., Oritani, K. and Matsuda, T. (2008) Physical and functional interactions between STAT3 and KAP1. Oncogene 27, 3054-3059 (Pubitemid 351668002)
28. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., O'Connor, T. and Yamamoto, M. (2003) Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 8, 379-391 (Pubitemid 36504013)
29. Nioi, P., McMahon, M., Itoh, K., Yamamoto, M. and Hayes, J. D. (2003) Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD(P)H:quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem. J. 374, 337-348
30. Prestera, T., Talalay, P., Alam, J., Ahn, Y. I., Lee, P. J. and Choi, A. M. (1995) Parallel induction of heme oxygenase-1 and chemoprotective phase 2 enzymes by electrophiles and antioxidants: regulation by upstream antioxidant-responsive elements (ARE). Mol. Med. 1, 827-837
31. Hu, G., Kim, J., Xu, Q., Leng, Y., Orkin, S. H. and Elledge, S. J. (2009) A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Gene Dev. 23, 837-848
32. Hayes, J. D., McMahon, M., Chowdhry, S. and Dinkova-Kostova, A. T. (2010) Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxid. Redox Signal 13, 1713-1748
33. Reichard, J. F., Motz, G. T. and Puga, A. (2007) Heme oxygenase-1 induction by NRF2 requires inactivation of the transcriptional repressor BACH1. Nucleic Acids Res. 35, 7074-7086
34. Alam, J., Camhi, S. and Choi, A. M. (1995) Identification of a second region upstream of the mouse heme oxygenase-1 gene that functions as a basal level and inducer-dependent transcription enhancer. J. Biol. Chem. 270, 11977-11984
35. Park, E. Y., Cho, I. J. and Kim, S. G. (2004) Transactivation of the PPAR-responsive enhancer module in chemopreventive glutathione S-transferase gene by the peroxisome proliferator-activated receptor-gamma and retinoid X receptor heterodimer. Cancer Res. 64, 3701-3713
36. Nguyen, T., Sherrat, P. J. and Pickett, C. B. (2003) Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43, 233-260
37. Sun, Z., Chi, Y. E. and Zhang, D. D. (2009) Acetylation of Nrf2 by p300/CBP augments promoter-specific DNA binding of Nrf2 during the antioxidant response. Mol. Cell. Biol. 29, 2658-2672
38. Ziv, Y., Bielopolski, D., Galanty, Y., Lukas, C., Taya, Y., Schultz, D. C., Lukas, J., Bekker-Jensen, S., Bartek, J. and Shiloh, Y. (2006) Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat. Cell Biol. 8, 870-876
39. Wolf, D. and Goff, S. P. (2007) TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 131, 46-57 (Pubitemid 47498526)
40. Wolf, D., Hug, K. and Goff, S. P. (2008) TRIM28 mediates primer binding site-targeted silencing of Lys1,2 tRNA-utilizing retroviruses in embryonic cells. Proc. Natl. Acad. Sci. U.S.A. 105, 12521-12526
41. Zhang, H.-S., Li, H.-Y., Zhou, Y., Wu, M.-R. and Zhou, H.-S. (2009) Nrf2 is involved in inhibiting Tat-induced HIV-1 long terminal repeat transactivation. Free Radical Biol. Med. 47, 261-268
42. Wu, R. F., Ma, Z., Myers, D. P. and Terada, L. S. (2007) HIV-1 Tat activates dual Nox pathways leading to independent activation of ERK and JNK MAP kinases. J. Biol. Chem. 282, 37412-37419
43. Qiang, W., Cahill, J. M., Liu, J., Kuang, X., Liu, N., Scofield, V. L., Voorhees, J. R., Reid, A. J., Yan, M., Lynn, W. S. and Wong, P. K. (2004) Activation of transcription factor Nrf-2 and its downstream targets in response to moloney murine leukemia virus ts1-induced thiol depletion and oxidative stress in astrocytes. J. Virol. 78, 11926-11938
44. Jakobsson, J., Cordero, M. I., Bisaz, R., Groner, A. C., Busskamp, V., Bensadoun, J. C., Cammas, F., Losson, R., Mansuy, I. M., Sandi, C. and Trono, D. (2008) KAP1-mediated epigenetic repression in the forebrain modulates behavioral vulnerability to stress. Neuron 60, 818-831
45. Johnson, J. A., Johnson, D. A, Kraft, A. D., Calkins, M. J., Jakel, R. J., Vargas, M. R. and Chen, P. C. (2008) The Nrf2-ARE pathway: an indicator and modulator of oxidative stress in neurodegeneration. Ann. NY Acad. Sci. 1147, 61-69