The C-Terminal domain of Nrf1 negatively regulates the full-length CNC-bZIP factor and its shorter isoform LCR-F1/Nrf1β; both are also inhibited by the small dominant-negative Nrf1γ/δ isoforms that down-regulate ARE-battery gene expression

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Zhang, Yiguo ^a   Qiu, Lu ^a   Li, Shaojun ^a   Xiang, Yuancai ^a   Chen, Jiayu ^a   Ren, Yonggang ^a  

^a CHONGQING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; TRANSCRIPTION FACTOR GAL4; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF1 BETA; TRANSCRIPTION FACTOR NRF1 DELTA; TRANSCRIPTION FACTOR NRF1 GAMMA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; ISOPROTEIN; NUCLEAR RESPIRATORY FACTOR 1; PROTEIN BINDING;

ANIMAL CELL; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHIMERA; COMPETITIVE INHIBITION; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM MEMBRANE; GENE EXPRESSION; NONHUMAN; PROTEIN DOMAIN; TRANSACTIVATION; UPREGULATION; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMISTRY; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; MUTATION; REPORTER GENE; SEQUENCE ALIGNMENT; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL LINE; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENES, REPORTER; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR RESPIRATORY FACTOR 1; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN ISOFORMS; SEQUENCE ALIGNMENT; TRANSCRIPTIONAL ACTIVATION;

EID: 84907817553     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109159     Document Type: Article

References (71)

1. Sykiotis GP, Bohmann D (2010) Stress-activated cap'n'collar transcription factors in aging and human disease. Sci. Signal. 3, re3.
2. Koch A, Steffen J, Kruger E (2011) TCF11 at the crossroads of oxidative stress and the ubiquitin proteasome system. Cell Cycle 10, 1200-1207.
3. Steffen J, Seeger M, Koch A, Kruger E (2010) Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol. Cell 40, 147-158.
4. Radhakrishnan SK, Lee CS, Young P, Beskow A, Chan JY, et al. (2010) Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell 38, 17-28.
5. Grimberg KB, Beskow A, Lundin D, Davis MM, Young P (2011) Basic leucine zipper protein Cnc-C is a substrate and transcriptional regulator of the Drosophila 26S proteasome. Mol. Cell Biol. 31, 897-909.
6. Li X, Matilainen O, Jin C, Glover-Cutter KM, Holmberg CI, et al. (2011) Specific SKN-1/Nrf stress responses to perturbations in translation elongation and proteasome activity. PLoS Genet. 7, e1002119.
7. Rushmore TH, Morton MR, Pickett CB (1991) The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 266, 11632-11639.
8. Bean TL, Ney PA (1997) Multiple regions of p45 NF-E2 are required for β-globin gene expression in erythroid cells. Nucleic Acids Res. 25, 2509-2515.
9. Johnsen O, Murphy P, Prydz H, Kolsto AB (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.
10. Kwak MK, Kensler TW (2011) Targeting Nrf2 signaling for cancer chemoprevention. Toxicol. Appl. Pharmacol. 244, 66-76.
11. Zhang Y, Kobayashi A, Yamamoto M, Hayes JD (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.
12. Zhang Y, Lucocq JM, Hayes JD (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.
13. Higgins LG, Kelleher MO, Eggleston IM, Itoh K, Yamamoto M, et al. (2009) Transcription factor Nrf2 mediates an adaptive response to sulforaphane that protects fibroblasts in vitro against the cytotoxic effects of electrophiles, peroxides and redox-cycling agents. Toxicol. Appl. Pharmacol. 237, 267-280.
14. Xiao H, Lu F, Stewart D, Zhang Y (2013) Mechanisms underlying chemopreventive effects of flavonoids via multiple signaling nodes within Nrf2-ARE and AhR-XRE gene regulatory networks. Curr. Chem. Biol. 7, 151-176.
15. Chan K, Lu R, Chang JC, Kan YW (1996) Nrf2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc. Natl. Acad. Sci. USA 93, 13943-13948.
16. Xu C, Huang MT, Shen G, Yuan X, Lin W, et al. (2006) Inhibition of 7, 12-dimethylbenz (a) anthracene-induced skin tumorigenesis in C57BL/6 mice by sulforaphane is mediated by nuclear factor E2-related factor 2. Cancer Res. 66, 8293-8296.
17. Leung L, Kwong M, Hou S, Lee C, Chan JY (2003) Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress. J. Biol. Chem. 278, 48021-48029.
18. Farmer SC, Sun CW, Winnier GE, Hogan BL, Townes TM (1997) The bZIP transcription factor LCR-F1 is essential for mesoderm formation in mouse development. Genes Dev. 11, 786-798.
19. Chan JY, Kwong M, Lu R, Chang J, Wang B, et al. (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.
20. Kwong M, Kan YW, Chan JY (1999) The CNC basic leucine zipper factor, Nrf1, is essential for cell survival in response to oxidative stress-inducing agents. Role for Nrf1 in γ-gcs (l) and gss expression in mouse fibroblasts. J. Biol. Chem. 274, 37491-37498.
21. Xu Z, Chen L, Leung L, Yen TS, Lee C, et al. (2005) Liver-specific inactivation of the Nrf1 gene in adult mouse leads to nonalcoholic steatohepatitis and hepatic neoplasia. Proc. Natl. Acad. Sci. USA 102, 4120-4125.
22. Ohtsuji M, Katsuoka F, Kobayashi A, Aburatani H, Hayes JD, et al. (2008) Nrf1 and Nrf2 play distinct roles in activation of antioxidant response elementdependent genes. J. Biol. Chem. 283, 33554-33562.
23. Kobayashi A, Tsukide T, Miyasaka T, Morita T, Mizoroki T, et al. (2011) Central nervous system-specific deletion of transcription factor Nrf1 causes progressive motor neuronal dysfunction. Genes Cells 16, 692-703.
24. Lee CS, Lee C, Hu T, Nguyen JM, Zhang J, et al. (2011) Loss of nuclear factor E2-related factor 1 in the brain leads to dysregulation of proteasome gene expression and neurodegeneration. Proc. Natl. Acad. Sci. USA 108, 8408-8413.
25. Kim J, Xing W, Wergedal J, Chan JY, Mohan S (2010) Targeted disruption of nuclear factor erythroid-derived 2-like 1 in osteoblasts reduces bone size and bone formation in mice. Physiol. Genomics 40, 100-110.
26. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, et al. (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13, 76-86.
27. Wang H, Liu K, Geng M, Gao P, Wu X, et al. (2013) RXRα inhibits the Nrf2-ARE signaling pathway through a direct interaction with the Neh7 domain of NRF2. Cancer Res. 73, 3097-3108.
28. Rupert PB, Daughdrill GW, Bowerman B, Matthews BW (1998) A new DNA-binding motif in the Skn-1 binding domain-DNA complex. Nat. Struct. Biol. 5, 484-491.
29. Kusunoki H, Motohashi H, Katsuoka F, Morohashi A, Yamamoto M, et al. (2002) Solution structure of the DNA-binding domain of MafG. Nat. Struct. Biol. 9, 252-256.
30. McMahon M, Itoh K, Yamamoto M, Hayes JD (2003) Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J. Biol. Chem. 278, 21592-21600.
31. Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, et al. (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.
32. Tong KI, Kobayashi A, Katsuoka F, Yamamoto M (2006) Two-site substrate recognition model for the Keap1-Nrf2 system: a hinge and latch mechanism. Biol. Chem. 387, 1311-1320.
33. Padmanabhan B, Tong KI, Ohta T, Nakamura Y, Scharlock M, et al. (2006) Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol. Cell 21, 689-700.
34. McMahon M, Thomas N, Itoh K, Yamamoto M, Hayes JD (2006) Dimerization of substrate adaptors can facilitate cullin-mediated ubiquitylation of proteins by a "tethering" mechanism: a two-site interaction model for the Nrf2-Keap1 complex. J. Biol. Chem. 281, 24756-24768.
35. Lo SC, Li X, Henzl MT, Beamer LJ, Hannink M (2006) Structure of the Keap1:Nrf2 interface provides mechanistic insight into Nrf2 signaling. EMBO J. 25, 3605-3617.
36. Ogura T, Tong KI, Mio K, Maruyama Y, Kurokawa H, et al. (2010) Keap1 is a forked-stem dimer structure with two large spheres enclosing the intervening, double glycine repeat, and C-terminal domains. Proc. Natl. Acad. Sci. USA 107, 2842-2847.
37. Nioi P, Nguyen T, Sherratt PJ, Pickett CB (2005) The carboxy-terminal Neh3 domain of Nrf2 is required for transcriptional activation. Mol. Cell Biol. 25, 10895-10906.
38. Katoh Y, Itoh K, Yoshida E, Miyagishi M, Fukamizu A, et al. (2001) Two domains of Nrf2 cooperatively bind CBP, a CREB binding protein, and synergistically activate transcription. Genes Cells 6, 857-868.
39. Zhang J, Hosoya T, Maruyama A, Nishikawa K, Maher JM, et al. (2007) Nrf2 Neh5 domain is differentially utilized in the transactivation of cytoprotective genes. Biochem. J. 404, 459-466.
40. Kim JH, Yu S, Chen JD, Kong AN (2012) The nuclear cofactor RAC3/AIB1 SRC-3 enhances Nrf2 signaling by interacting with transactivation domains. Oncogene 32, 514-527.
41. McMahon M, Thomas N, Itoh K, Yamamoto M, Hayes JD (2004) Redoxregulated turnover of Nrf2 is determined by at least two separate protein domains, the redox-sensitive Neh2 degron and the redox-insensitive Neh6 degron. J. Biol. Chem. 279, 31556-31567.
42. Chowdhry S, Zhang Y, McMahon M, Sutherland C, Cuadrado A, et al. (2013) Nrf2 is controlled by two distinct β-TrCP recognition motifs in its Neh6 domain, one of which can be modulated by GSK-3 activity. Oncogene 32, 3765-3781.
43. Zhang Y, Crouch DH, Yamamoto M, Hayes JD (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.
44. Zhang Y, Lucocq JM, Yamamoto M, Hayes JD (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.
45. Zhang Y, Ren Y, Li S, Hayes JD (2014) Transcription factor Nrf1 is topologically repartitioned across membranes to enable target gene transactivation through its acidic glucose-responsive domains. PLoS One 9, 1-17 (e93456); doi:93410.93137/journal.pone.0093456.
46. Zhang Y, Hayes JD (2013) The membrane-topogenic vectorial behaviour of Nrf1 controls its post-translational modification and transactivation activity. Sci. Rep. 3:2006, 1-16, doi:10.1038/srep02006.
47. Wang W, Chan JY (2006) Nrf1 is targeted to the endoplasmic reticulum membrane by an N-terminal transmembrane domain. Inhibition of nuclear translocation and transacting function. J. Biol. Chem. 281, 19676-19687.
48. Zhang Y, Li S, Xiang Y, Zhao H, Hayes JD (2014) The selective posttranslational processing of Nrf1 yields distinct isoforms that dictate its activity to differentially regulate target genes. (In press of Sci. Rep. MS-13-05858).
49. Chan JY, Han XL, Kan YW (1993) Cloning of Nrf1, an NF-E2-related transcription factor, by genetic selection in yeast. Proc. Natl. Acad. Sci. USA 90, 11371-11375.
50. Luna L, Johnsen O, Skartlien AH, Pedeutour F, Turc-Carel C, et al. (1994) Molecular cloning of a putative novel human bZIP transcription factor on chromosome 17q22. Genomics 22, 553-562.
51. Tsuchiya Y, Morita T, Kim M, Iemura S, Natsume T, et al. (2011) Dual Regulation of the Transcriptional Activity of Nrf1 by beta-TrCP- and Hrd1-Dependent Degradation Mechanisms. Mol. Cell Biol. 31, 4500-4512.
52. Zhong Y, Fang S (2012) Live cell imaging of protein dislocation from the endoplasmic reticulum. J. Biol. Chem. 287, 28057-28066.
53. Zhang Y, Mattjus P, Schmid PC, Dong ZM, Zhong S, et al. (2001) Involvement of the acid sphingomyelinase pathway in UVA-induced apoptosis. J. Biol. Chem. 276, 11775-11782.
54. Chen L, Kwong M, Lu R, Ginzinger D, Lee C, et al. (2003) Nrf1 is critical for redox balance and survival of liver cells during development. Mol. Cell Biol. 23, 4673-4686.
55. Yang H, Magilnick N, Lee C, Kalmaz D, Ou X, et al. (2005) Nrf1 and Nrf2 Regulate Rat Glutamate-Cysteine Ligase Catalytic Subunit Transcription Indirectly via NF-kB and AP-1. Mol. Cell Biol. 25, 5933-5946.
56. Hirotsu Y, Hataya N, Katsuoka F, Yamamoto M (2012) NF-E2-related factor 1 (Nrf1) serves as a novel regulator of hepatic lipid metabolism through regulation of the Lipin1 and PGC-1β genes. Mol. Cell Biol. 32, 2760-2770.
57. Novotny V, Prieschl EE, Csonga R, Fabjani G, Baumruker T (1998) Nrf1 in a complex with fosB, c-jun, junD and ATF2 forms the AP1 component at the TNFα promoter in stimulated mast cells. Nucleic Acids Res. 26, 5480-5485.
58. Prieschl EE, Novotny V, Csonga R, Jaksche D, Elbe-Burger A, et al. (1998) A novel splice variant of the transcription factor Nrf1 interacts with the TNFα promoter and stimulates transcription. Nucleic Acids Res 26, 2291-2297.
59. Zhang Y (2009) Molecular and cellular control of the Nrf1 transcription factor: An integral membrane glycoprotein. VDM Verlag Dr. Müller Publishing House Germany (May 2009). The first edition, pp1-264.
60. Chepelev NL, Bennitz JD, Huang T, McBride S, Willmore WG (2011) The Nrf1 CNC-bZIP protein is regulated by the proteasome and activated by hypoxia. PLoS One 6, e29167.
61. Caterina JJ, Donze D, Sun CW, Ciavatta DJ, Townes TM (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.
62. Wang W, Kwok AM, Chan JY (2007) The p65 isoform of Nrf1 is a dominant negative inhibitor of ARE-mediated transcription. J. Biol. Chem. 282, 24670-24678.
63. Kwong EK, Kim KM, Penalosa PJ, Chan JY (2012) Characterization of Nrf1b, a novel isoform of the nuclear factor-erythroid-2 related transcription factor-1 that activates antioxidant response element-regulated genes. PLoS One 7, e48404.
64. Schultz MA, Hagan SS, Datta A, Zhang Y, Freeman ML, et al. (2014) Nrf1 and nrf2 transcription factors regulate androgen receptor transactivation in prostate cancer cells. PLoS One 9, e87204.
65. Herskowitz I (1987) Functional inactivation of genes by dominant negative mutations. Nature 329, 219-222.
66. Sakurai A, Miyamoto T, Refetoff S, DeGroot LJ (1990) Dominant negative transcriptional regulation by a mutant thyroid hormone receptor-beta in a family with generalized resistance to thyroid hormone. Mol. Endocrinol. 4, 1988-1994.
67. Johnsen O, Skammelsrud N, Luna L, Nishizawa M, Prydz H, et al. (1996) Small Maf proteins interact with the human transcription factor TCF11/Nrf1/LCR-F1. Nucleic Acids Res. 24, 4289-4297.
68. Husberg C, Murphy P, Martin E, Kolsto AB (2001) Two domains of the human bZIP transcription factor TCF11 are necessary for transactivation. J. Biol. Chem. 276, 17641-17652.
69. Huang CF, Wang YC, Tsao DA, Tung SF, Lin YS, et al. (2000) Antagonism between members of the CNC-bZIP family and the immediate-early protein IE2 of human cytomegalovirus. J. Biol. Chem. 275, 12313-12320.
70. Wu JL, Lin YS, Yang CC, Lin YJ, Wu SF, et al. (2009) MCRS2 represses the transactivation activities of Nrf1. BMC Cell Biol. 10, 9.
71. Tsuchiya Y, Taniguchi H, Ito Y, Morita T, Karim MR, et al. (2013) The CK2-Nrf1 axis controls the clearance of ubiquitinated proteins by regulating proteasome gene expression. Mol. Cell Biol. 33, 3461-3472.