Nrf1 CNC-bZIP protein promotes cell survival and nucleotide excision repair through maintaining glutathione homeostasis

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 18788-18795

  Han, Weinong ^a   Ming, Mei ^a   Zhao, Rui ^b,c   Pi, Jingbo ^b   Wu, Chunli ^a,c   He, Yu Ying ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

^c CHINA MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT RESPONSE; BCL-2 FAMILY; CELL SURVIVAL; DNA DAMAGES; DNA LESIONS; DNA REPAIR; ENVIRONMENTAL RISK FACTOR; GLUTATHIONES; HUMAN SKIN; ISOFORMS; KERATINOCYTES; MOUSE SKIN; NORMAL SKIN; NUCLEAR FACTORS; NUCLEOTIDE EXCISION REPAIR; REPAIR PATHWAYS; SKIN CANCERS; TUMOR SUPPRESSORS; UVB RADIATION;

CELLS; CHEMICAL COMPOUNDS; CYTOLOGY; DNA; GENES; NUCLEOTIDES; PEPTIDES; TRANSCRIPTION; TRANSCRIPTION FACTORS; TUMORS;

REPAIR;

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; BCL 2 INTERACTING KILLER; GENOMIC DNA; GLUTATHIONE; MESSENGER RNA; PROTEIN BCL 2; TRANSCRIPTION FACTOR NRF1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP C PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BCL 2 INTERACTING KILLER GENE; CANCER INHIBITION; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; EXCISION REPAIR; GENE; GENE EXPRESSION REGULATION; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIATION RESPONSE; RADIOSENSITIZATION; SKIN CARCINOGENESIS; SKIN CARCINOMA; TRANSCRIPTION REGULATION; ULTRAVIOLET B RADIATION; UPREGULATION; XERODERMA PIGMENTOSUM GROUP C GENE;

CELL SURVIVAL; DNA REPAIR; GLUTATHIONE; HOMEOSTASIS; HUMANS; NUCLEAR PROTEINS; NUCLEAR RESPIRATORY FACTOR 1; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 84861551463     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.363614     Document Type: Article

References (46)

1. Bowden, G. T. (2004) Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signaling. Nat. Rev. Cancer 4, 23-35
2. Johnson, T. M., Dolan, O. M., Hamilton, T. A., Lu, M. C., Swanson, N. A., and Lowe, L. (1998) Clinical and histologic trends of melanoma. J. Am. Acad. Dermatol. 38, 681-686 (Pubitemid 28213709)
3. Jans, J., Schul, W., Sert, Y. G., Rijksen, Y., Rebel, H., Eker, A. P., Nakajima, S., van Steeg, H., de Gruijl, F. R., Yasui, A., Hoeijmakers, J. H., and van der Horst, G. T. (2005) Powerful skin cancer protection by a CPD-photolyase transgene. Curr. Biol. 15, 105-115
4. Cleaver, J. E. (2005) Cancer in xeroderma pigmentosum and related disorders of DNA repair. Nat. Rev. Cancer 5, 564-573
5. Cleaver, J. E., Lam, E. T., and Revet, I. (2009) Disorders of nucleotide excision repair: the genetic and molecular basis of heterogeneity. Nat. Rev. Genet. 10, 756-768
6. Kraemer, K. H. (1997) Sunlight and skin cancer: another link revealed. Proc. Natl. Acad. Sci. U.S.A. 94, 11-14
7. Hoeijmakers, J. H. (2001) Genome maintenance mechanisms for preventing cancer. Nature 411, 366-374
8. Volker, M., Moné, M. J., Karmakar, P., van Hoffen, A., Schul, W., Vermeulen, W., Hoeijmakers, J. H., van Driel, R., van Zeeland, A. A., and Mullenders, L. H. (2001) Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8, 213-224 (Pubitemid 32772919)
9. Sugasawa, K., Ng, J. M., Masutani, C., Iwai, S., van der Spek, P. J., Eker, A. P., Hanaoka, F., Bootsma, D., and Hoeijmakers, J. H. (1998) Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell 2, 223-232 (Pubitemid 128373647)
10. Riedl, T., Hanaoka, F., and Egly, J. M. (2003) The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J. 22, 5293-5303 (Pubitemid 37222048)
11. Chan, J. Y., Han, X. L., and Kan, Y. W. (1993) Cloning of Nrf1, an NF-E2-related transcription factor, by genetic selection in yeast. Proc. Natl. Acad. Sci. U.S.A. 90, 11371-11375 (Pubitemid 23354431)
12. Andrews, N. C., Erdjument-Bromage, H., Davidson, M. B., Tempst, P., and Orkin, S. H. (1993) Erythroid transcription factor NF-E2 is a hematopoietic-specific basic leucine zipper protein. Nature 362, 722-728 (Pubitemid 23125974)
13. Kobayashi, A., Ito, E., Toki, T., Kogame, K., Takahashi, S., Igarashi, K., Hayashi, N., and Yamamoto, M. (1999) Molecular cloning and functional characterization of a new Cap'n' collar family transcription factor Nrf3. J. Biol. Chem. 274, 6443-6452 (Pubitemid 29111059)
14. Moi, P., Chan, K., Asunis, I., Cao, A., and Kan, Y. W. (1994) Isolation of NF-E2-related factor 2 (Nrf2), an NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the β-globin locus control region. Proc. Natl. Acad. Sci. U.S.A. 91, 9926-9930 (Pubitemid 24311921)
15. Oyake, T., Itoh, K., Motohashi, H., Hayashi, N., Hoshino, H., Nishizawa, M., Yamamoto, M., and Igarashi, K. (1996) Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol. Cell Biol. 16, 6083-6095 (Pubitemid 26360968)
16. Zhang, D. D. (2006) Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug. Metab. Rev. 38, 769-789
17. Pi, J., Freeman, M. L., and Yamamoto, M. (2010) Nrf2 in toxicology and pharmacology: the good, the bad, and the ugly? Toxicol. Appl. Pharmacol. 244, 1-3
18. Luna, L., Johnsen, O., Skartlien, A. H., Pedeutour, F., Turc-Carel, C., Prydz, H., and Kolstø, A. B. (1994) Molecular cloning of a putative novel human bZIP transcription factor on chromosome 17q22. Genomics 22, 553-562 (Pubitemid 24273983)
19. Murphy, P., and Kolstø, A. (2000) Expression of the bZIP transcription factor TCF11 and its potential dimerization partners during development. Mech. Dev. 97, 141-148
20. Venugopal, R., and Jaiswal, A. K. (1996) Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc. Natl. Acad. Sci. U.S.A. 93, 14960-14965 (Pubitemid 26419078)
21. Johnsen, O., Murphy, P., Prydz, H., and Kolsto, A. B. (1998) Interaction of the CNC-bZIP factor TCF11/LCR-F1/Nrf1 with MafG: binding-site selection and regulation of transcription. Nucleic Acids Res. 26, 512-520 (Pubitemid 28291577)
22. Nioi, P., and Hayes, J. D. (2004) Contribution of NAD(P)H:quinone oxidoreductase 1 to protection against carcinogenesis, and regulation of its gene by the Nrf2 basic region leucine zipper and the arylhydrocarbon receptor basic helix-loop-helix transcription factors. Mutat. Res. 555, 149-171 (Pubitemid 39359178)
23. Chen, L., Kwong, M., Lu, R., Ginzinger, D., Lee, C., Leung, L., and Chan, J. Y. (2003) Nrf1 is critical for redox balance and survival of liver cells during development. Mol. Cell Biol. 23, 4673-4686 (Pubitemid 36734755)
24. Leung, L., Kwong, M., Hou, S., Lee, C., and Chan, J. Y. (2003) Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress. J. Biol. Chem. 278, 48021-48029 (Pubitemid 37523252)
25. Yang, H., Magilnick, N., Lee, C., Kalmaz, D., Ou, X., Chan, J. Y., and Lu, S. C. (2005) Nrf1 and Nrf2 regulate rat glutamate-cysteine ligase catalytic subunit transcription indirectly via NF- ≲καππα∀B and AP-1. Mol. Cell Biol. 25, 5933-5946 (Pubitemid 40949988)
26. Ohtsuji, M., Katsuoka, F., Kobayashi, A., Aburatani, H., Hayes, J. D., and Yamamoto, M. (2008) Nrf1 and Nrf2 play distinct roles in activation of antioxidant response element-dependent genes. J. Biol. Chem. 283, 33554-33562
27. Zhao, R., Hou, Y., Xue, P., Woods, C. G., Fu, J., Feng, B., Guan, D., Sun, G., Chan, J. Y., Waalkes, M. P., Andersen, M. E., and Pi, J. (2011) Long isoforms of NRF1 contribute to arsenic-induced antioxidant response in human keratinocytes. Environ. Health Perspect. 119, 56-62
28. Maeda, T., Chua, P. P., Chong, M. T., Sim, A. B., Nikaido, O., and Tron, V. A. (2001) Nucleotide excision repair genes are up-regulated by low-dose artificial ultraviolet B: evidence of a photoprotective SOS response? J. Invest. Dermatol. 117, 1490-1497 (Pubitemid 34032778)
29. Shimazu, T., Degenhardt, K., Nur-E-Kamal, A., Zhang, J., Yoshida, T., Zhang, Y., Mathew, R., White, E., and Inouye, M. (2007) NBK/BIK antagonizes MCL-1 and BCL-XL and activates BAK-mediated apoptosis in response to protein synthesis inhibition. Gene Dev. 21, 929-941 (Pubitemid 46625642)
30. Youle, R. J., and Strasser, A. (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9, 47-59
31. Daniel, P. T., Pun, K. T., Ritschel, S., Sturm, I., Holler, J., Dörken, B., and Brown, R. (1999) Expression of the death gene Bik/Nbk promotes sensitivity to drug-induced apoptosis in corticosteroid-resistant T-cell lymphoma and prevents tumor growth in severe combined immunodeficient mice. Blood 94, 1100-1107 (Pubitemid 29361843)
32. Real, P. J., Sanz, C., Gutierrez, O., Pipaon, C., Zubiaga, A. M., and Fernandez-Luna, J. L. (2006) Transcriptional activation of the proapoptotic bik gene by E2F proteins in cancer cells. FEBS Lett. 580, 5905-5909 (Pubitemid 44584291)
33. Radhakrishnan, S. K., Lee, C. S., Young, P., Beskow, A., Chan, J. Y., and Deshaies, R. J. (2010) Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell 38, 17-28
34. Cam, H., Balciunaite, E., Blais, A., Spektor, A., Scarpulla, R. C., Young, R., Kluger, Y., and Dynlacht, B. D. (2004) A common set of gene regulatory networks links metabolism and growth inhibition. Mol. Cell 16, 399-411 (Pubitemid 39504794)
35. Dominguez-Brauer, C., Chen, Y. J., Brauer, P. M., Pimkina, J., and Raychaudhuri, P. (2009) ARF stimulates XPC to trigger nucleotide excision repair by regulating the repressor complex of E2F4. EMBO Rep. 10, 1036-1042
36. Ming, M., Shea, C. R., Guo, X., Li, X., Soltani, K., Han, W., and He, Y. Y. (2010) Regulation of global genome nucleotide excision repair by SIRT1 through xeroderma pigmentosum C. Proc. Natl. Acad. Sci. U.S.A. 107, 22623-22628
37. Ming, M., Feng, L., Shea, C. R., Soltani, K., Zhao, B., Han, W., Smart, R. C., Trempus, C. S., and He, Y. Y. (2011) PTEN positively regulates UVB-induced DNA damage repair. Cancer Res. 71, 5287-5295
38. Zahedi Avval, F., and Holmgren, A. (2009) Molecular mechanisms of thioredoxin and glutaredoxin as hydrogen donors for mammalian S phase ribonucleotide reductase. J. Biol. Chem. 284, 8233-8240
39. Markovic, J., Borrás, C., Ortega, A., Sastre, J., Viña, J., and Pallardó, F. V. (2007) Glutathione is recruited into the nucleus in early phases of cell proliferation. J. Biol. Chem. 282, 20416-20424 (Pubitemid 47099986)
40. Markovic, J., Mora, N. J., Broseta, A. M., Gimeno, A., de-la-Concepción, N., Viña, J., and Pallardó, F. V. (2009) The depletion of nuclear glutathione impairs cell proliferation in 3t3 fibroblasts. PLoS One 4, e6413
41. Xu, Z., Chen, L., Leung, L., Yen, T. S., Lee, C., and Chan, J. Y. (2005) Liver-specific inactivation of the Nrf1 gene in adult mouse leads to non-alcoholic steatohepatitis and hepatic neoplasia. Proc. Natl. Acad. Sci. U.S.A. 102, 4120-4125 (Pubitemid 40388565)
42. Marín, M. S., López-Cima, M. F., García-Castro, L., Pascual, T., Marrón, M. G., and Tardón, A. (2004) Poly (AT) polymorphism in intron 11 of the XPCDNArepair gene enhances the risk of lung cancer. Cancer Epidemiol. Biomarkers Prev. 13, 1788-1793
43. Hollander, M. C., Philburn, R. T., Patterson, A. D., Velasco-Miguel, S., Friedberg, E. C., Linnoila, R. I., and Fornace, A. J., Jr. (2005) Deletion of XPC leads to lung tumors in mice and is associated with early events in human lung carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 102, 13200-13205 (Pubitemid 41325001)
44. Lee, G. Y., Jang, J. S., Lee, S. Y., Jeon, H. S., Kim, K. M., Choi, J. E., Park, J. M., Chae, M. H., Lee, W. K., Kam, S., Kim, I. S., Lee, J. T., Jung, T. H., and Park, J. Y. (2005) XPC polymorphisms and lung cancer risk. Int. J. Cancer 115, 807-813 (Pubitemid 40776705)
45. Hu, Z., Wang, Y., Wang, X., Liang, G., Miao, X., Xu, Y., Tan, W., Wei, Q., Lin, D., and Shen, H. (2005) DNA repair gene XPC genotypes/haplotypes and risk of lung cancer in a Chinese population. Int. J. Cancer 115, 478-483 (Pubitemid 40663754)
46. Zhu, Y., Lai, M., Yang, H., Lin, J., Huang, M., Grossman, H. B., Dinney, C. P., and Wu, X. (2007) Genotypes, haplotypes, and diplotypes of XPC and risk of bladder cancer. Carcinogenesis 28, 698-703 (Pubitemid 46523367)