Home LiteratureArticle Details
PMID: 20452972 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription.

The Journal of biological chemistry ·Vol. 285 ·No. 29 ·2010-07-16 ·Pages 22576-91

Jain A, Lamark T, Sjøttem E, Larsen KB, Awuh JA, Øvervatn A, McMahon M, Hayes JD, Johansen T

Abstract

The p62/SQSTM1 (sequestosome 1) protein, which acts as a cargo receptor for autophagic degradation of ubiquitinated targets, is up-regulated by various stressors. Induction of the p62 gene by oxidative stress is mediated by NF-E2-related factor 2 (NRF2) and, at the same time, p62 protein contributes to the activation of NRF2, but hitherto the mechanisms involved were not known. Herein, we have mapped an antioxidant response element (ARE) in the p62 promoter that is responsible for its induction by oxidative stress via NRF2. Chromatin immunoprecipitation and gel mobility-shift assays verified that NRF2 binds to this cis-element in vivo and in vitro. Also, p62 docks directly onto the Kelch-repeat domain of Kelch-like ECH-associated protein 1 (KEAP1), via a motif designated the KEAP1 interacting region (KIR), thereby blocking binding between KEAP1 and NRF2 that leads to ubiquitylation and degradation of the transcription factor. The KIR motif in p62 is located immediately C-terminal to the LC3-interacting region (LIR) and resembles the ETGE motif utilized by NRF2 for its interaction with KEAP1. KIR is required for p62 to stabilize NRF2, and inhibition of KEAP1 by p62 occurs from a cytoplasmic location within the cell. The LIR and KIR motifs cannot be engaged simultaneously by LC3 and KEAP1, but because p62 is polymeric the interaction between KEAP1 and p62 leads to accumulation of KEAP1 in p62 bodies, which is followed by autophagic degradation of KEAP1. Our data explain how p62 contributes to activation of NRF2 target genes in response to oxidative stress through creating a positive feedback loop.

MeSH Terms
Adaptor Proteins, Signal Transducing/chemistry,genetics,metabolism Amino Acid Sequence Animals Antioxidants/metabolism Autophagy Base Sequence Binding Sites Binding, Competitive Feedback, Physiological Gene Expression Regulation HeLa Cells Heat-Shock Proteins/chemistry,genetics,metabolism Humans Inclusion Bodies/metabolism Intracellular Signaling Peptides and Proteins/metabolism Kelch-Like ECH-Associated Protein 1 Mice Microtubule-Associated Proteins/metabolism Molecular Sequence Data NF-E2-Related Factor 2/metabolism Protein Binding Protein Processing, Post-Translational Response Elements/genetics Sequestosome-1 Protein Signal Transduction/genetics Transcription, Genetic
Chemicals
Adaptor Proteins, Signal Transducing Antioxidants Heat-Shock Proteins Intracellular Signaling Peptides and Proteins KEAP1 protein, human Kelch-Like ECH-Associated Protein 1 MAP1LC3A protein, human Microtubule-Associated Proteins NF-E2-Related Factor 2 SQSTM1 protein, human Sequestosome-1 Protein Sqstm1 protein, mouse
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Jain Ashish
Molecular Cancer Research Group, Institute of Medical Biology, University of Tromsø, 9037 Tromsø, Norway.
Lamark Trond
Sjøttem Eva
Larsen Kenneth Bowitz
Awuh Jane Atesoh
Øvervatn Aud
McMahon Michael
Hayes John D
Johansen Terje
References (63)
63 references, click to expand
  1. A genomic screen for activators of the antioxidant response element.
    Proc Natl Acad Sci U S A. 2007 Mar 20;104(12):5205-10 PMID: 17360324
  2. p62 at the crossroads of autophagy, apoptosis, and cancer.
    Cell. 2009 Jun 12;137(6):1001-4 PMID: 19524504
  3. Interaction of protein kinase C zeta with ZIP, a novel protein kinase C-binding protein.
    Proc Natl Acad Sci U S A. 1997 Jun 10;94(12):6191-6 PMID: 9177193
  4. The atypical PKC-interacting protein p62 channels NF-kappaB activation by the IL-1-TRAF6 pathway.
    EMBO J. 2000 Apr 3;19(7):1576-86 PMID: 10747026
  5. Nrf2 controls constitutive and inducible expression of ARE-driven genes through a dynamic pathway involving nucleocytoplasmic shuttling by Keap1.
    J Biol Chem. 2005 Sep 16;280(37):32485-92 PMID: 16000310
  6. Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling.
    Cell. 2009 May 15;137(4):721-35 PMID: 19427028
  7. Autophagy suppresses tumorigenesis through elimination of p62.
    Cell. 2009 Jun 12;137(6):1062-75 PMID: 19524509
  8. Mapping of atypical protein kinase C within the nerve growth factor signaling cascade: relationship to differentiation and survival of PC12 cells.
    Mol Cell Biol. 2000 Jul;20(13):4494-504 PMID: 10848576
  9. The basic region and leucine zipper transcription factor MafK is a new nerve growth factor-responsive immediate early gene that regulates neurite outgrowth.
    J Neurosci. 2002 Oct 15;22(20):8971-80 PMID: 12388604
  10. 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. 2003 Nov;23(22):8137-51 PMID: 14585973
  11. Sequestosome 1/p62 links familial ALS mutant SOD1 to LC3 via an ubiquitin-independent mechanism.
    J Neurochem. 2009 Nov;111(4):1062-73 PMID: 19765191
  12. Predictive base substitution rules that determine the binding and transcriptional specificity of Maf recognition elements.
    Genes Cells. 2006 Jun;11(6):575-91 PMID: 16716189
  13. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway.
    Annu Rev Pharmacol Toxicol. 2007;47:89-116 PMID: 16968214
  14. Genetic evidence that small maf proteins are essential for the activation of antioxidant response element-dependent genes.
    Mol Cell Biol. 2005 Sep;25(18):8044-51 PMID: 16135796
  15. Keap1 regulates the oxidation-sensitive shuttling of Nrf2 into and out of the nucleus via a Crm1-dependent nuclear export mechanism.
    Mol Cell Biol. 2005 Jun;25(11):4501-13 PMID: 15899855
  16. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates.
    Mol Cell. 2009 Feb 27;33(4):505-16 PMID: 19250911
  17. The nuclear factor SPBP contains different functional domains and stimulates the activity of various transcriptional activators.
    J Biol Chem. 2000 Dec 22;275(51):40288-300 PMID: 10995766
  18. Molecular basis distinguishing the DNA binding profile of Nrf2-Maf heterodimer from that of Maf homodimer.
    J Biol Chem. 2007 Nov 16;282(46):33681-33690 PMID: 17875642
  19. Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway.
    Mol Cell Biol. 2003 Dec;23(23):8786-94 PMID: 14612418
  20. p62 overexpression in breast tumors and regulation by prostate-derived Ets factor in breast cancer cells.
    Oncogene. 2003 Apr 17;22(15):2322-33 PMID: 12700667
  21. Physical and functional interaction of sequestosome 1 with Keap1 regulates the Keap1-Nrf2 cell defense pathway.
    J Biol Chem. 2010 May 28;285(22):16782-8 PMID: 20378532
  22. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2.
    Mol Cell Biol. 2004 Aug;24(16):7130-9 PMID: 15282312
  23. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1.
    Nat Cell Biol. 2010 Mar;12(3):213-23 PMID: 20173742
  24. NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets.
    Cell Cycle. 2009 Jul 1;8(13):1986-90 PMID: 19502794
  25. Molecular cloning of a phosphotyrosine-independent ligand of the p56lck SH2 domain.
    Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5991-5 PMID: 8650207
  26. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice.
    Cell. 2007 Dec 14;131(6):1149-63 PMID: 18083104
  27. The signaling adaptor p62 is an important NF-kappaB mediator in tumorigenesis.
    Cancer Cell. 2008 Apr;13(4):343-54 PMID: 18394557
  28. Role of Nrf2 and p62/ZIP in the neurite outgrowth by carnosic acid in PC12h cells.
    J Biochem. 2010 Jan;147(1):73-81 PMID: 19762340
  29. Nucleocytoplasmic shuttling of p62/SQSTM1 and its role in recruitment of nuclear polyubiquitinated proteins to promyelocytic leukemia bodies.
    J Biol Chem. 2010 Feb 19;285(8):5941-53 PMID: 20018885
  30. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins.
    J Biol Chem. 2003 Sep 5;278(36):34568-81 PMID: 12813044
  31. The ePHD protein SPBP interacts with TopBP1 and together they co-operate to stimulate Ets1-mediated transcription.
    Nucleic Acids Res. 2007;35(19):6648-62 PMID: 17913746
  32. Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxidant response.
    Mol Cell. 2009 Jun 26;34(6):663-73 PMID: 19560419
  33. Signal integration and diversification through the p62 scaffold protein.
    Trends Biochem Sci. 2007 Feb;32(2):95-100 PMID: 17174552
  34. Increased expression of p62 in expanded polyglutamine-expressing cells and its association with polyglutamine inclusions.
    J Neurochem. 2004 Oct;91(1):57-68 PMID: 15379887
  35. Structure of the Keap1:Nrf2 interface provides mechanistic insight into Nrf2 signaling.
    EMBO J. 2006 Aug 9;25(15):3605-17 PMID: 16888629
  36. 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. 2003 Sep 1;374(Pt 2):337-48 PMID: 12816537
  37. Keap1 recruits Neh2 through binding to ETGE and DLG motifs: characterization of the two-site molecular recognition model.
    Mol Cell Biol. 2006 Apr;26(8):2887-900 PMID: 16581765
  38. Autophagy fights disease through cellular self-digestion.
    Nature. 2008 Feb 28;451(7182):1069-75 PMID: 18305538
  39. Novel cytoprotective mechanism of anti-parkinsonian drug deprenyl: PI3K and Nrf2-derived induction of antioxidative proteins.
    Biochem Biophys Res Commun. 2006 Jan 20;339(3):915-22 PMID: 16325767
  40. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy.
    J Biol Chem. 2007 Aug 17;282(33):24131-45 PMID: 17580304
  41. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death.
    J Cell Biol. 2005 Nov 21;171(4):603-14 PMID: 16286508
  42. Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2.
    Mol Cell Biol. 2007 Sep;27(18):6334-49 PMID: 17636022
  43. Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression.
    J Biol Chem. 2003 Jun 13;278(24):21592-600 PMID: 12682069
  44. Low micromolar levels of hydrogen peroxide and proteasome inhibitors induce the 60-kDa A170 stress protein in murine peritoneal macrophages.
    Biochem Biophys Res Commun. 1997 Mar 6;232(1):33-7 PMID: 9125146
  45. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress.
    J Biol Chem. 2009 May 15;284(20):13291-5 PMID: 19182219
  46. Oxidative damage to the promoter region of SQSTM1/p62 is common to neurodegenerative disease.
    Neurobiol Dis. 2009 Aug;35(2):302-10 PMID: 19481605
  47. Rapid screening for improved solubility of small human proteins produced as fusion proteins in Escherichia coli.
    Protein Sci. 2002 Feb;11(2):313-21 PMID: 11790841
  48. Structural basis for sorting mechanism of p62 in selective autophagy.
    J Biol Chem. 2008 Aug 15;283(33):22847-57 PMID: 18524774
  49. Chemical and molecular regulation of enzymes that detoxify carcinogens.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2965-9 PMID: 8385353
  50. p62/SQSTM1 and ALFY interact to facilitate the formation of p62 bodies/ALIS and their degradation by autophagy.
    Autophagy. 2010 Apr;6(3):330-44 PMID: 20168092
  51. 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. 2006 Aug 25;281(34):24756-68 PMID: 16790436
  52. Nrf2-Keap1 defines a physiologically important stress response mechanism.
    Trends Mol Med. 2004 Nov;10(11):549-57 PMID: 15519281
  53. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase.
    Mol Cell Biol. 2004 Oct;24(19):8477-86 PMID: 15367669
  54. Localization of atypical protein kinase C isoforms into lysosome-targeted endosomes through interaction with p62.
    Mol Cell Biol. 1998 May;18(5):3069-80 PMID: 9566925
  55. The interaction of p62 with RIP links the atypical PKCs to NF-kappaB activation.
    EMBO J. 1999 Jun 1;18(11):3044-53 PMID: 10356400
  56. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages.
    J Biol Chem. 2000 May 26;275(21):16023-9 PMID: 10821856
  57. p62, a phosphotyrosine-independent ligand of the SH2 domain of p56lck, belongs to a new class of ubiquitin-binding proteins.
    J Biol Chem. 1996 Aug 23;271(34):20235-7 PMID: 8702753
  58. Subcellular localization and cytoplasmic complex status of endogenous Keap1.
    Genes Cells. 2007 Oct;12(10):1163-78 PMID: 17903176
  59. Nuclear oncoprotein prothymosin alpha is a partner of Keap1: implications for expression of oxidative stress-protecting genes.
    Mol Cell Biol. 2005 Feb;25(3):1089-99 PMID: 15657435
  60. Integration and diversity of the regulatory network composed of Maf and CNC families of transcription factors.
    Gene. 2002 Jul 10;294(1-2):1-12 PMID: 12234662
  61. The ubiquitin-binding protein p62 is expressed in breast cancers showing features of aggressive disease.
    Endocr Relat Cancer. 2007 Mar;14(1):73-80 PMID: 17395976
  62. Cytosolic overexpression of p62 sequestosome 1 in neoplastic prostate tissue.
    Histopathology. 2006 Jan;48(2):157-61 PMID: 16405664
  63. NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer.
    Trends Biochem Sci. 2009 Apr;34(4):176-88 PMID: 19321346
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2010-07-16
Epub
2010-00-07
Pages
22576-91
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2903417
Subset
IM
Grants
Cancer Research UK · C4909/A9990 · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com