Oxidant-induced cell death and Nrf2-dependent antioxidative response are controlled by Fra-1/AP-1

Molecular and Cellular Biology

Volumn 32, Issue 9, 2012, Pages 1694-1709

  Vaz, Michelle ^a   Machireddy, Narsa ^a,c   Irving, Ashley ^a   Potteti, Haranatha R ^a   Chevalier, Karinne ^a,c   Kalvakolanu, Dhananjaya ^b   Reddy, Sekhar P ^a,c  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIQUAT; ENZYME; GLUTATHIONE; HMOX1 PROTEIN; NQO1 PROTEIN; OXIDIZING AGENT; PROTEIN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FRA 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; CELL DEATH; EMBRYO; EMBRYO CELL; GENE EXPRESSION; LUNG FIBROBLAST; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; RNA INTERFERENCE; WILD TYPE;

ANIMALS; CELL DEATH; CELLS, CULTURED; FIBROBLASTS; LUNG; MICE; MICE, KNOCKOUT; MITOCHONDRIAL MEMBRANES; NF-E2-RELATED FACTOR 2; OXIDANTS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-FOS; TRANSCRIPTION FACTOR AP-1;

EID: 84861401086     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.06390-11     Document Type: Article

References (60)

1. Behrens A, Sibilia M, Wagner EF. 1999. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet. 21:326-329.
2. Bowler RP, Barnes PJ, Crapo JD. 2004. The role of oxidative stress in chronic obstructive pulmonary disease. COPD 1:255-277.
3. Burch PM, Yuan Z, Loonen A, Heintz NH. 2004. An extracellular signal-regulated kinase 1-and 2-dependent program of chromatin trafficking of c-Fos and Fra-1 is required for cyclin D1 expression during cell cycle reentry. Mol. Cell. Biol. 24:4696-4709.
4. Casalino L, et al. 2007. Fra-1 promotes growth and survival in RAStransformed thyroid cells by controlling cyclin A transcription. EMBO J. 26:1878-1890.
5. Chinenov Y, Kerppola TK. 2001. Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 20:2438-2452.
6. Cho HY, et al. 2002. Role of NRF2 in protection against hyperoxic lung injury in mice. Am. J. Respir. Cell Mol. Biol. 26:175-182.
7. Ciencewicki J, Trivedi S, Kleeberger SR. 2008. Oxidants and the pathogenesis of lung diseases. J. Allergy Clin. Immunol. 122:456-468.
8. Cohen DR, Curran T. 1988. fra-1: a serum-inducible, cellular immediateearly gene that encodes a fos-related antigen. Mol. Cell. Biol. 8:2063-2069.
9. DeNicola GM, et al. 2011. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475:106-109.
10. Dhakshinamoorthy S, Jain AK, Bloom DA, Jaiswal AK. 2005. Bach1 competes with Nrf2 leading to negative regulation of the antioxidant response element (ARE)-mediated NAD(P)H:quinone oxidoreductase 1 gene expression and induction in response to antioxidants. J. Biol. Chem. 280:16891-16900.
11. Eferl R, et al. 2004. The Fos-related antigen Fra-1 is an activator of bone matrix formation. EMBO J. 23:2789-2799.
12. Eferl R, et al. 1999. Functions of c-Jun in liver and heart development. J. Cell Biol. 145:1049-1061.
13. Eferl R, Wagner EF. 2003. AP-1: a double-edged sword in tumorigenesis. Nat. Rev. Cancer 3:859-868.
14. Estus S, et al. 1994. Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J. Cell Biol. 127:1717-1727.
15. Finkel T. 2003. Oxidant signals and oxidative stress. Curr. Opin. Cell Biol. 15:247-254.
16. Finkel T, Holbrook NJ. 2000. Oxidants, oxidative stress and the biology of ageing. Nature 408:239-247.
17. Gerald D, et al. 2004. JunD reduces tumor angiogenesis by protecting cells from oxidative stress. Cell 118:781-794.
18. Hafezi F, et al. 1997. The absence of c-fos prevents light-induced apoptotic cell death of photoreceptors in retinal degeneration in vivo. Nat. Med. 3:346-349.
19. Hai T, Curran T. 1991. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc. Natl. Acad. Sci. U. S. A. 88:3720-3724.
20. Ham J, et al. 1995. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14:927-939.
21. He CH, et al. 2001. Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. J. Biol. Chem. 276:20858-20865.
22. Igarashi K, et al. 1994. Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins. Nature 367:568-572.
23. Itoh K, et al. 1997. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236:313-322.
24. Itoh K, Ishii T, Wakabayashi N, Yamamoto M. 1999. Regulatory mechanisms of cellular response to oxidative stress. Free Radic. Res. 31:319-324.
25. Itoh K, Mimura J, Yamamoto M. 2010. Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxid. Redox. Signal. 13: 1665-1678.
26. Itoh K, et al. 2003. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 8:379-391.
27. Jeyapaul J, Jaiswal AK. 2000. Nrf2 and c-Jun regulation of antioxidant response element (ARE)-mediated expression and induction of gammaglutamylcysteine synthetase heavy subunit gene. Biochem. Pharmacol. 59: 1433-1439.
28. Karapetian RN, et al. 2005. Nuclear oncoprotein prothymosin alpha is a partner of Keap1: implications for expression of oxidative stressprotecting genes. Mol. Cell. Biol. 25:1089-1099.
29. Karin M, Liu Z, Zandi E. 1997. AP-1 function and regulation. Curr. Opin. Cell Biol. 9:240-246.
30. Karin M, Shaulian E. 2001. AP-1: linking hydrogen peroxide and oxida-tive stress to the control of cell proliferation and death. IUBMB Life 52:17-24.
31. Katsuoka F, et al. 2005. Genetic evidence that small maf proteins are essential for the activation of antioxidant response element-dependent genes. Mol. Cell. Biol. 25:8044-8051.
32. Kensler TW, Wakabayashi N, Biswal S. 2007. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47:89-116.
33. Kobayashi M, Yamamoto M. 2006. Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv. Enzyme Regul. 46:113-140.
34. Kolbus A, et al. 2000. c-Jun-dependent CD95-L expression is a ratelimiting step in the induction of apoptosis by alkylating agents. Mol. Cell. Biol. 20:575-582.
35. MacLaren A, Black EJ, Clark W, Gillespie DA. 2004. c-Jun-deficient cells undergo premature senescence as a result of spontaneous DNA damage accumulation. Mol. Cell. Biol. 24:9006-9018.
36. Meixner A, Karreth F, Kenner L, Penninger JM, Wagner EF. 2010. Jun and JunD-dependent functions in cell proliferation and stress response. Cell Death Differ. 17:1409-1419.
37. Moi P, Chan K, Asunis I, Cao A, Kan YW. 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 beta-globin locus control region. Proc. Natl. Acad. Sci. U. S. A. 91:9926-9930.
38. Nguyen T, Sherratt PJ, Nioi P, Yang CS, Pickett CB. 2005. Nrf2 controls constitutive and inducible expression of ARE-driven genes through a dynamic pathway involving nucleocytoplasmic shuttling by Keap1. J. Biol. Chem. 280:32485-32492.
39. Osburn WO, et al. 2006. Nrf2 regulates an adaptive response protecting against oxidative damage following diquat-mediated formation of superoxide anion. Arch. Biochem. Biophys. 454:7-15.
40. Oyake T, et al. 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.
41. Reddy SP, Mossman BT. 2002. Role and regulation of activator protein-1 in toxicant-induced responses of the lung. Am. J. Physiol. Lung Cell Mol. Physiol. 283:L1161-L1178.
42. 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.
43. Ryter SW, et al. 2007. Mechanisms of cell death in oxidative stress. Antioxid. Redox. Signal. 9:49-89.
44. Schreiber M, Baumann B, Cotten M, Angel P, Wagner EF. 1995. Fos is an essential component of the mammalian UV response. EMBO J. 14: 5338-5349.
45. Shaulian E, Karin M. 2002. AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4:E131-E136.
46. Shaulian E, Karin M. 2001. AP-1 in cell proliferation and survival. Oncogene 20:2390-2400.
47. Sun J, et al. 2004. Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network. Proc. Natl. Acad. Sci. U. S. A. 101:1461-1466.
48. Sun Z, Zhang S, Chan JY, Zhang DD. 2007. Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2. Mol. Cell. Biol. 27:6334-6349.
49. Suzuki H, et al. 2004. Heme regulates gene expression by triggering Crm1-dependent nuclear export of Bach1. EMBO J. 23:2544-2553.
50. Suzuki H, et al. 2003. Cadmium induces nuclear export of Bach1, a transcriptional repressor of heme oxygenase-1 gene. J. Biol. Chem. 278: 49246-49253.
51. Takada Y, et al. 2011. Interstitial lung disease induced by gefitinib and Toll-like receptor ligands is mediated by Fra-1. Oncogene 30:3821-3832.
52. Talalay P, Dinkova-Kostova AT. 2004. Role of nicotinamide quinone oxidoreductase 1 (NQO1) in protection against toxicity of electrophiles and reactive oxygen intermediates. Methods Enzymol. 382:355-364.
53. Thimmulappa RK, et al. 2006. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J. Clin. Invest. 116:984-995.
54. Vaz M, Reddy NM, Subbiah R, Reddy SP. 2012. Genetic disruption of Fra-1 decreases susceptibility to endotoxin-induced acute lung injury and mortality in mice. Am. J. Respir. Cell Mol. Biol. 46:55-62.
55. Venugopal R, Jaiswal AK. 1998. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 17:3145-3156.
56. Verheij M, et al. 1996. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 380:75-79.
57. Vile GF, Basu-Modak S, Waltner C, Tyrrell RM. 1994. Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 91:2607-2610.
58. Weitzman JB, Fiette L, Matsuo K, Yaniv M. 2000. JunD protects cells from p53-dependent senescence and apoptosis. Mol. Cell 6:1109-1119.
59. Wisdom R, Johnson RS, Moore C. 1999. c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J. 18:188-197.
60. Yang H, et al. 2005. Nrf1 and Nrf2 regulate rat glutamate-cysteine ligase catalytic subunit transcription indirectly via NF-kappaB and AP-1. Mol. Cell. Biol. 25:5933-5946.