Home LiteratureArticle Details
PMID: 14673141 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Transcription factor Nrf2 regulates inflammation by mediating the effect of 15-deoxy-Delta(12,14)-prostaglandin j(2).

Molecular and cellular biology ·Vol. 24 ·No. 1 ·2004-01-00 ·Pages 36-45

Itoh K, Mochizuki M, Ishii Y, Ishii T, Shibata T, Kawamoto Y, Kelly V, Sekizawa K, Uchida K, Yamamoto M

Abstract

Activated macrophages express high levels of Nrf2, a transcription factor that positively regulates the gene expression of antioxidant and detoxication enzymes. In this study, we examined how Nrf2 contributes to the anti-inflammatory process. As a model system of acute inflammation, we administered carrageenan to induce pleurisy and found that in Nrf2-deficient mice, tissue invasion by neutrophils persisted during inflammation and the recruitment of macrophages was delayed. Using an antibody against 15-deoxy-Delta(12,14)-prostaglandin J(2) (15d-PGJ(2)), it was observed that macrophages from pleural lavage accumulate 15d-PGJ(2). We show that in mouse peritoneal macrophages 15d-PGJ(2) can activate Nrf2 by forming adducts with Keap1, resulting in an Nrf2-dependent induction of heme oxygenase 1 and peroxiredoxin I (PrxI) gene expression. Administration of the cyclooxygenase 2 inhibitor NS-398 to mice with carrageenan-induced pleurisy caused persistence of neutrophil recruitment and, in macrophages, attenuated the 15d-PGJ(2) accumulation and PrxI expression. Administration of 15d-PGJ(2) into the pleural space of NS-398-treated wild-type mice largely counteracted both the decrease in PrxI and persistence of neutrophil recruitment. In contrast, these changes did not occur in the Nrf2-deficient mice. These results demonstrate that Nrf2 regulates the inflammation process downstream of 15d-PGJ(2) by orchestrating the recruitment of inflammatory cells and regulating the gene expression within those cells.

MeSH Terms
Animals Cyclooxygenase 2 DNA-Binding Proteins/metabolism Hepatocytes Inflammation/metabolism Isoenzymes/metabolism Macrophages/metabolism Mice NF-E2-Related Factor 2 Peritoneum/metabolism Pleurisy/metabolism Prostaglandin D2/analogs & derivatives,metabolism Prostaglandin-Endoperoxide Synthases/metabolism Trans-Activators/metabolism
Chemicals
15-deoxy-delta(12,14)-prostaglandin J2 DNA-Binding Proteins Isoenzymes NF-E2-Related Factor 2 Nfe2l2 protein, mouse Trans-Activators Cyclooxygenase 2 Prostaglandin-Endoperoxide Synthases Prostaglandin D2
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Itoh Ken
ERATO Environmental Response Project, University of Tsukuba, Tsukuba 305-8577, Japan.
Mochizuki Mie
Ishii Yukio
Ishii Tetsuro
Shibata Takahiro
Kawamoto Yoshiyuki
Kelly Vincent
Sekizawa Kiyohisa
Uchida Koji
Yamamoto Masayuki
References (46)
46 references, click to expand
  1. Biological actions of delta 12-prostaglandin J2.
    J Lipid Mediat Cell Signal. 1995 Oct;12(2-3):443-8 PMID: 8777585
  2. Studies on the mediators of the acute inflammatory response induced in rats in different sites by carrageenan and turpentine.
    J Pathol. 1971 May;104(1):15-29 PMID: 4398139
  3. 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. 1996 Nov 26;93(24):13943-8 PMID: 8943040
  4. 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. 1996 Dec 10;93(25):14960-5 PMID: 8962164
  5. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements.
    Biochem Biophys Res Commun. 1997 Jul 18;236(2):313-22 PMID: 9240432
  6. Role of macrophage migration inhibitory factor in the regulation of the immune response.
    Adv Immunol. 1997;66:197-223 PMID: 9328642
  7. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation.
    Nature. 1998 Jan 1;391(6662):79-82 PMID: 9422508
  8. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines.
    Nature. 1998 Jan 1;391(6662):82-6 PMID: 9422509
  9. Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-alpha.
    J Biol Chem. 1998 Mar 13;273(11):6297-302 PMID: 9497357
  10. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain.
    Genes Dev. 1999 Jan 1;13(1):76-86 PMID: 9887101
  11. Inducible cyclooxygenase may have anti-inflammatory properties.
    Nat Med. 1999 Jun;5(6):698-701 PMID: 10371510
  12. Nonsteroid drug selectivities for cyclo-oxygenase-1 rather than cyclo-oxygenase-2 are associated with human gastrointestinal toxicity: a full in vitro analysis.
    Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7563-8 PMID: 10377455
  13. 15-deoxy-delta 12,14-prostaglandin J2. A prostaglandin D2 metabolite generated during inflammatory processes.
    J Biol Chem. 2002 Mar 22;277(12):10459-66 PMID: 11786541
  14. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs.
    Nat New Biol. 1971 Jun 23;231(25):232-5 PMID: 5284360
  15. Roles of Nrf2 in activation of antioxidant enzyme genes via antioxidant responsive elements.
    Methods Enzymol. 2002;348:182-90 PMID: 11885271
  16. Site and mechanism of growth inhibition by prostaglandins. III. Distribution and binding of prostaglandin A2 and delta 12-prostaglandin J2 in nuclei.
    J Pharmacol Exp Ther. 1987 Jul;242(1):306-11 PMID: 3302206
  17. Identification of a common chemical signal regulating the induction of enzymes that protect against chemical carcinogenesis.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8261-5 PMID: 3141925
  18. Biological activities and mechanisms of action of PGJ2 and related compounds: an update.
    Prostaglandins Leukot Essent Fatty Acids. 1992 Sep;47(1):1-12 PMID: 1438462
  19. The electrophile counterattack response: protection against neoplasia and toxicity.
    Adv Enzyme Regul. 1993;33:281-96 PMID: 8356913
  20. Cloning and characterization of a 23-kDa stress-induced mouse peritoneal macrophage protein.
    J Biol Chem. 1993 Sep 5;268(25):18633-6 PMID: 8360158
  21. Pharmacological and biochemical demonstration of the role of cyclooxygenase 2 in inflammation and pain.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12013-7 PMID: 7991575
  22. Heme oxygenase: a novel target for the modulation of the inflammatory response.
    Nat Med. 1996 Jan;2(1):87-90 PMID: 8564848
  23. The cyclopentenone prostaglandin 15-deoxy-Delta(12,14)-prostaglandin J(2) attenuates the development of acute and chronic inflammation.
    Mol Pharmacol. 2002 May;61(5):997-1007 PMID: 11961117
  24. Activation of the mouse heme oxygenase-1 gene by 15-deoxy-Delta(12,14)-prostaglandin J(2) is mediated by the stress response elements and transcription factor Nrf2.
    Antioxid Redox Signal. 2002 Apr;4(2):249-57 PMID: 12006176
  25. Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound.
    Mol Cell Biol. 2002 Aug;22(15):5492-505 PMID: 12101242
  26. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants.
    Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11908-13 PMID: 12193649
  27. Points of control in inflammation.
    Nature. 2002 Dec 19-26;420(6917):846-52 PMID: 12490957
  28. Laminar flow induction of antioxidant response element-mediated genes in endothelial cells. A novel anti-inflammatory mechanism.
    J Biol Chem. 2003 Jan 10;278(2):703-11 PMID: 12370194
  29. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles.
    Genes Cells. 2003 Apr;8(4):379-91 PMID: 12653965
  30. Induction of heme oxygenase-1 expression in murine macrophages is essential for the anti-inflammatory effect of low dose 15-deoxy-Delta 12,14-prostaglandin J2.
    J Biol Chem. 2003 May 23;278(21):19325-30 PMID: 12642589
  31. Nrf2 is essential for protection against acute pulmonary injury in mice.
    Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12731-6 PMID: 10535991
  32. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IkappaB kinase.
    Nature. 2000 Jan 6;403(6765):103-8 PMID: 10638762
  33. Cyclopentenone prostaglandins-new allies in the war on inflammation.
    Nat Med. 2000 Feb;6(2):137-8 PMID: 10655096
  34. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway.
    Nat Med. 2000 Apr;6(4):422-8 PMID: 10742149
  35. 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
  36. Resolution of inflammation.
    Int J Immunopharmacol. 2000 Dec;22(12):1131-5 PMID: 11137620
  37. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes.
    Toxicol Sci. 2001 Jan;59(1):169-77 PMID: 11134556
  38. 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. 2001 Mar 13;98(6):3410-5 PMID: 11248092
  39. Regulation of macrophage migration inhibitory factor and thiol-specific antioxidant protein PAG by direct interaction.
    J Biol Chem. 2001 May 4;276(18):15504-10 PMID: 11297517
  40. Accelerated DNA adduct formation in the lung of the Nrf2 knockout mouse exposed to diesel exhaust.
    Toxicol Appl Pharmacol. 2001 Jun 15;173(3):154-60 PMID: 11437637
  41. Induction of cellular antioxidative stress genes through heterodimeric transcription factor Nrf2/small Maf by antirheumatic gold(I) compounds.
    J Biol Chem. 2001 Sep 7;276(36):34074-81 PMID: 11429414
  42. 15-Deoxy-Delta 12,14-prostaglandin J2 inhibition of NF-kappaB-DNA binding through covalent modification of the p50 subunit.
    J Biol Chem. 2001 Sep 21;276(38):35530-6 PMID: 11466314
  43. Nrf2-deficient female mice develop lupus-like autoimmune nephritis.
    Kidney Int. 2001 Oct;60(4):1343-53 PMID: 11576348
  44. MIF regulates innate immune responses through modulation of Toll-like receptor 4.
    Nature. 2001 Dec 20-27;414(6866):920-4 PMID: 11780066
  45. Role of NRF2 in protection against hyperoxic lung injury in mice.
    Am J Respir Cell Mol Biol. 2002 Feb;26(2):175-82 PMID: 11804867
  46. Antioxidant-inducible genes.
    Adv Pharmacol. 1997;38:293-328 PMID: 8895814
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2004-01-00
Pages
36-45
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC303336
Subset
IM
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