Identification of topological determinants in the N-terminal domain of transcription factor Nrf1 that control its orientation in the endoplasmic reticulum membrane

Biochemical Journal

Volumn 430, Issue 3, 2010, Pages 497-510

  Zhang, Yiguo ^a,b   Hayes, John D ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b CHONGQING UNIVERSITY   (China)

Author keywords

Detergent resistant membrane; Endoplasmic reticulum; N glycosylation; NF E2 (nuclear factor erythroid 2) related factor 1 (Nrf1); Nuclear envelope; Topology

Indexed keywords

AMINO ACIDS; CYTOLOGY; DETERGENTS; ESTERIFICATION; GLYCOSYLATION; ORGANIC ACIDS; PEPTIDES; TOPOLOGY; TRANSCRIPTION; TRANSCRIPTION FACTORS;

DETERGENT-RESISTANT MEMBRANES; ENDOPLASMIC RETICULUM; N-GLYCOSYLATION; NUCLEAR ENVELOPE; NUCLEAR FACTORS;

MEMBRANES;

N TERMINAL HOMOLOGY BOX 2; PROTEIN; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR NRF1; UNCLASSIFIED DRUG; LUCIFERASE; MUTANT PROTEIN; NRF1 PROTEIN, MOUSE; NUCLEAR RESPIRATORY FACTOR 1;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS MEMBRANE; CONSENSUS SEQUENCE; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; ANIMAL; BINDING SITE; CHLOROCEBUS AETHIOPS; CONFOCAL MICROSCOPY; COS 1 CELL LINE; GENETICS; GLYCOSYLATION; METABOLISM; MOLECULAR GENETICS; MOUSE; MUTAGENESIS; MUTATION; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BLOTTING, WESTERN; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOPLASM; ENDOPLASMIC RETICULUM; GLYCOSYLATION; LUCIFERASES; MICE; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTANT PROTEINS; MUTATION; NUCLEAR RESPIRATORY FACTOR 1; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 77956661152     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100471     Document Type: Article

References (57)

1. 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
2. Luna, L., Johnsen, O., Skartlien, A. H., Pedeutour, F., Turc-Carel, C., Prydz, H. and Kolsto, A. B. (1994) Molecular cloning of a putative novel human bZIP transcription factor on chromosome 17q22. Genomics 22, 553-562
3. Moi, P., Chan, K., Asunis, I., Cao, A. and Kan, Y. W. (1994) Isolation of NF-E2-related factor 2 (Nrf2), a 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
4. 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
5. 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
6. 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
7. 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
8. Zhang, Y., Kobayashi, A., Yamamoto, M. and Hayes, J. D. (2009) The Nrf3 transcription factor is a membrane-bound glycoprotein targeted to the endoplasmic reticulum through its N-terminal homology box 1 sequence. J. Biol. Chem. 284, 3195-3210
9. 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
10. 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
11. 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-κB and AP-1. Mol. Cell. Biol. 25, 5933-5946
12. McMahon, M., Itoh, K., Yamamoto, M., Chanas, S. A., Henderson, C. J., McLellan, L. I., Wolf, C. R., Cavin, C. and Hayes, J. D. (2001) The Cap 'n' Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res. 61, 3299-3307
13. Chanas, S. A., Jiang, Q., McMahon, M., McWalter, G. K., McLellan, L. I., Elcombe, C. R., Henderson, C. J., Wolf, C. R., Moffat, G. J., Itoh, K. et al. (2002) Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice. Biochem. J. 365, 405-416
14. Kensler, T. W., Wakabayashi, N. and Biswal, S. (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47, 89-116
15. 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
16. Murphy, P. and Kolsto, A. (2000) Expression of the bZIP transcription factor TCF11 and its potential dimerization partners during development. Mech. Dev. 97, 141-148
17. Kobayashi, A., Ohta, T. and Yamamoto, M. (2004) Unique function of the Nrf2-Keap1 pathway in the inducible expression of antioxidant and detoxifying enzymes. Methods Enzymol. 378, 273-286 (Pubitemid 38248581)
18. Etchevers, H. C. (2005) The cap 'n' collar family member NF-E2-related factor 3 (Nrf3) is expressed in mesodermal derivatives of the avian embryo. Int. J. Dev. Biol. 49, 363-367
19. Farmer, S. C., Sun, C. W., Winnier, G. E., Hogan, B. L. and Townes, T. M. (1997) The bZIP transcription factor LCR-F1 is essential for mesoderm formation in mouse development. Genes Dev. 11, 786-798
20. Chan, J. Y., Kwong, M., Lu, R., Chang, J., Wang, B., Yen, T. S. and Kan, Y. W. (1998) Targeted disruption of the ubiquitous CNC-bZIP transcription factor, Nrf-1, results in anemia and embryonic lethality in mice. EMBO J. 17, 1779-1787
21. Kwong, M., Kan, Y. W. and Chan, J. Y. (1999) The CNC basic leucine zipper factor, Nrf1, is essential for cell survival in response to oxidative stress-inducing agents. Role for Nrf1 in g-gcs(l) and gss expression in mouse fibroblasts. J. Biol. Chem. 274, 37491-37498
22. 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 nonalcoholic steatohepatitis and hepatic neoplasia. Proc. Natl. Acad. Sci. U.S.A. 102, 4120-4125
23. Chan, K., Lu, R., Chang, J. C. and Kan, Y. W. (1996) NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc. Natl. Acad. Sci. U.S.A. 93, 13943-13948
24. 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
25. 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
26. Rangasamy, T., Guo, J., Mitzner, W. A., Roman, J., Singh, A., Fryer, A. D., Yamamoto, M., Kensler, T. W., Tuder, R. M., Georas, S. N. and Biswal, S. (2005) Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice. J. Exp. Med. 202, 47-59
27. 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
28. Chowdhry, S., Nazmy, M. H., Meakin, P. J., Dinkova-Kostova, A. T., Walsh, S. V., Tsujita, T., Dillon, J. F., Ashford, M. L. and Hayes, J. D. (2010) Loss of Nrf2 markedly exacerbates nonalcoholic steatohepatitis. Free Radical Biol. Med. 48, 357-371
29. Derjuga, A., Gourley, T. S., Holm, T. M., Heng, H. H., Shivdasani, R. A., Ahmed, R., Andrews, N. C. and Blank, V. (2004) Complexity of CNC transcription factors as revealed by gene targeting of the Nrf3 locus. Mol. Cell. Biol. 24, 3286-3294
30. Luna, L., Skammelsrud, N., Johnsen, O., Abel, K. J., Weber, B. L., Prydz, H. and Kolsto, A. B. (1995) Structural organization and mapping of the human TCF11 gene. Genomics 27, 237-244
31. Caterina, J. J., Donze, D., Sun, C. W., Ciavatta, D. J. and Townes, T. M. (1994) Cloning and functional characterization of LCR-F1: a bZIP transcription factor that activates erythroid-specific, human globin gene expression. Nucleic Acids Res. 22, 2383-2391
32. Husberg, C., Murphy, P., Martin, E. and Kolsto, A. B. (2001) Two domains of the human bZIP transcription factor TCF11 are necessary for transactivation. J. Biol. Chem. 276, 17641-17652
33. Zhang, Y., Lucocq, J. M., Yamamoto, M. and Hayes, J. D. (2007) The NHB1 (N-terminal homology box 1) sequence in transcription factor Nrf1 is required to anchor it to the endoplasmic reticulum and also to enable its asparagine-glycosylation. Biochem. J. 408, 161-172
34. Zhang, Y. (2009) Molecular and cellular control of the Nrf1 transcription factor: an integral membrane glycoprotein, Vdm Verlag Dr Müller Publishing House, Germany
35. Zhang, Y., Lucocq, J. M. and Hayes, J. D. (2009) The Nrf1 CNC/bZIP protein is a nuclear envelope-bound transcription factor that is activated by t-butyl hydroquinone but not by endoplasmic reticulum stressors. Biochem. J. 418, 293-310
36. Zhang, Y., Crouch, D. H., Yamamoto, M. and Hayes, J. D. (2006) Negative regulation of the Nrf1 transcription factor by its N-terminal domain is independent of Keap1: Nrf1, but not Nrf2, is targeted to the endoplasmic reticulum. Biochem. J. 399, 373-385
37. Zhang, Y., Cho, Y. Y., Petersen, B. L., Bode, A. M., Zhu, F. and Dong, Z. (2003) Ataxia telangiectasia mutated proteins, MAPKs, and RSK2 are involved in the phosphorylation of STAT3. J. Biol. Chem. 278, 12650-12659
38. Wang, X. J., Hayes, J. D. and Wolf, C. R. (2006) Generation of a stable antioxidant response element-driven reporter gene cell line and its use to show redox-dependent activation of nrf2 by cancer chemotherapeutic agents. Cancer Res. 66, 10983-10994
39. van Geest, M. and Lolkema, J. S. (2000) Membrane topology and insertion of membrane proteins: search for topogenic signals. Microbiol. Mol. Biol. Rev. 64, 13-33
40. Zhang, Y., Zhong, S., Dong, Z., Chen, N., Bode, A. M., Ma, W. and Dong, Z. (2001) UVA induces Ser381 phosphorylation of p90RSK/MAPKAP-K1 via ERK and JNK pathways. J. Biol. Chem. 276, 14572-14580
41. Zhang, Y., Mattjus, P., Schmid, P. C., Dong, Z., Zhong, S., Ma, W. Y., Brown, R. E., Bode, A. M., Schmid, H. H. and Dong, Z. (2001) Involvement of the acid sphingomyelinase pathway in UVA-induced apoptosis. J. Biol. Chem. 276, 11775-11782
42. Millen, J. I., Pierson, J., Kvam, E., Olsen, L. J. and Goldfarb, D. S. (2008) The luminal N-terminus of yeast Nvj1 is an inner nuclear membrane anchor. Traffic 9, 1653-1664
43. Kahn, R. A. (2009) Toward a model for Arf GTPases as regulators of traffic at the Golgi. FEBS Lett. 583, 3872-3879
44. Inoue, H. and Randazzo, P. A. (2007) Arf GAPs and their interacting proteins. Traffic 8, 1465-1475
45. Nie, Z. and Randazzo, P. A. (2006) Arf GAPs and membrane traffic. J. Cell Sci. 119, 1203-1211
46. Paetzel, M., Karla, A., Strynadka, N. C. and Dalbey, R. E. (2002) Signal peptidases. Chem. Rev. 102, 4549-4580
47. Ott, C. M. and Lingappa, V. R. (2002) Integral membrane protein biosynthesis: why topology is hard to predict. J. Cell Sci. 115, 2003-2009
48. McMahon, H. T. and Gallop, J. L. (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590-596
49. Bowie, J. U. (2005) Solving the membrane protein folding problem. Nature 438, 581-589
50. von Heijne, G. (2006) Membrane-protein topology. Nat. Rev. Mol. Cell Biol. 7, 909-918
51. Dowhan, W. and Bogdanov, M. (2009) Lipid-dependent membrane protein topogenesis. Annu. Rev. Biochem. 78, 515-540
52. Johnson, A. E. (2009) The structural and functional coupling of two molecular machines, the ribosome and the translocon. J. Cell Biol. 185, 765-767
53. Skach, W. R. (2009) Cellular mechanisms of membrane protein folding. Nat. Struct. Mol. Biol. 16, 606-612
54. Epand, R. M., Sayer, B. G. and Epand, R. F. (2005) Caveolin scaffolding region and cholesterol-rich domains in membranes. J. Mol. Biol. 345, 339-350
55. Drin, G., Casella, J. F., Gautier, R., Boehmer, T., Schwartz, T. U. and Antonny, B. (2007) A general amphipathic α-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 14, 138-146
56. Phoenix, D. A., Harris, F., Daman, O. A. and Wallace, J. (2002) The prediction of amphiphilic α-helices. Curr. Protein Pept. Sci. 3, 201-221
57. Mesmin, B., Drin, G., Levi, S., Rawet, M., Cassel, D., Bigay, J. and Antonny, B. (2007) Two lipid-packing sensor motifs contribute to the sensitivity of ArfGAP1 to membrane curvature. Biochemistry 46, 1779-1790