Multiorgan autoimmune inflammation, enhanced lymphoproliferation, and impaired homeostasis of reactive oxygen species in mice lacking the antioxidant-activated transcription factor Nrf2.

Nuclear factor erythroid 2-related factor 2 (Nrf2) is an antioxidant-activated cap "n" collar basic leucine zipper transcription factor. To assess the function of Nrf2 in the antioxidant response, we examined mice with targeted disruption of the Nrf2 gene. Nrf2-null mice developed complex disease manifestations, with a majority exhibiting a lupus-like autoimmune syndrome characterized by multiorgan inflammatory lesions with a marked female predominance, appearance of anti-double-stranded DNA antibodies in young adulthood, intravascular deposition of immunoglobulin complexes in blood vessels, and premature death due to rapidly progressing membranoproliferative glomerular nephritis. Mechanistic analyses revealed that the null mice showed enhanced proliferative response of CD4+ T cells, altered ratios of CD4+ and CD8+ cells, and increased oxidative lesions in tissues. Analyses of antioxidant-induced gene expression showed that the knockout mice were devoid of the basal and inducible expression of certain phase 2 detoxification enzymes and antioxidant genes in hepatic and lymphoid cells in vivo. Our findings suggest that Nrf2 mediates important antioxidant functions involved in the control of peripheral lymphocyte homeostasis and autoimmune surveillance.

[1]  T. Behrens,et al.  Delineating the genetic basis of systemic lupus erythematosus. , 2001, Immunity.

[2]  S. Tonegawa,et al.  Heme oxygenase 1 is required for mammalian iron reutilization. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  M. Holsapple Autoimmunity by pesticides: a critical review of the state of the science. , 2002, Toxicology letters.

[4]  Y. Kan,et al.  Chromosomal localization of the human NF-E2 family of bZIP transcription factors by fluorescence in situ hybridization , 1995, Human Genetics.

[5]  Y. Kan,et al.  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. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[6]  E. Marshall Lupus: Mysterious Disease Holds Its Secrets Tight , 2002, Science.

[7]  T. Vyse,et al.  Genetic susceptibility to systemic lupus erythematosus. , 1998, Annual review of immunology.

[8]  Y. Kan,et al.  An important function of Nrf2 in combating oxidative stress: Detoxification of acetaminophen , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[9]  J. Mohler,et al.  Segmentally restricted, cephalic expression of a leucine zipper gene during Drosophila embryogenesis , 1991, Mechanisms of Development.

[10]  H. Masutani,et al.  Hemin-induced Activation of the Thioredoxin Gene by Nrf2 , 2001, The Journal of Biological Chemistry.

[11]  Paul Tempst,et al.  Erythroid transcription factor NF-E2 is a haematopoietic-specific basic–leucine zipper protein , 1993, Nature.

[12]  G. Cooper,et al.  Glutathione S-transferase M null homozygosity and risk of systemic lupus erythematosus associated with sun exposure: a possible gene-environment interaction for autoimmunity. , 2003, The Journal of rheumatology.

[13]  Jenny R. Roberts,et al.  Accelerated Ovarian Failure Induced by 4-Vinyl Cyclohexene Diepoxide in Nrf2 Null Mice , 2006, Molecular and Cellular Biology.

[14]  J. Ward,et al.  Progressive Glomerulonephritis and Histiocytic Sarcoma Associated with Macrophage Functional Defects in CYP1B1-Deficient Mice , 2004, Toxicologic pathology.

[15]  Y. Kan,et al.  Induction of murine NAD(P)H:quinone oxidoreductase by 2,3,7,8-tetrachlorodibenzo-p-dioxin requires the CNC (cap 'n' collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduc , 2004, The Biochemical journal.

[16]  C. B. Pickett,et al.  Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. , 2003, Annual review of pharmacology and toxicology.

[17]  Y. Kan,et al.  Cloning of Nrf1, an NF-E2-related transcription factor, by genetic selection in yeast. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[18]  K. Itoh,et al.  Nrf2-deficient female mice develop lupus-like autoimmune nephritis. , 2001, Kidney international.

[19]  Stefan F Martin,et al.  T Lymphocyte-Mediated Immune Responses to Chemical Haptens and Metal Ions: Implications for Allergic and Autoimmune Disease , 2004, International Archives of Allergy and Immunology.

[20]  B. Chandrasekar,et al.  Decreased pro-inflammatory cytokines and increased antioxidant enzyme gene expression by omega-3 lipids in murine lupus nephritis. , 1994, Biochemical and biophysical research communications.

[21]  Y. Kan,et al.  NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[22]  K. Itoh,et al.  Cloning and characterization of a novel erythroid cell-derived CNC family transcription factor heterodimerizing with the small Maf family proteins , 1995, Molecular and cellular biology.

[23]  R. Pieters,et al.  Chemical-specific properties co-determine the type of adverse immune response. , 2003, Autoimmunity reviews.

[24]  A. Choi,et al.  Identification of Activating Transcription Factor 4 (ATF4) as an Nrf2-interacting Protein , 2001, The Journal of Biological Chemistry.

[25]  F. Finkelman,et al.  The impact of T helper and T regulatory cells on the regulation of anti-double-stranded DNA B cells. , 2002, Immunity.

[26]  Y. Kan,et al.  Isolation of cDNA encoding the human NF-E2 protein. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[27]  M. Reth,et al.  The adaptor protein SLP-65 acts as a tumor suppressor that limits pre-B cell expansion , 2003, Nature Immunology.

[28]  D. D'cruz Autoimmune diseases associated with drugs, chemicals and environmental factors. , 2000, Toxicology letters.

[29]  M. Monestier,et al.  Mechanisms of heavy metal-induced autoimmunity. , 2005, Molecular immunology.

[30]  K. Itoh,et al.  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 , 1996, Molecular and cellular biology.

[31]  M. Kwak,et al.  Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  S. Reddy,et al.  Role of NRF2 in protection against hyperoxic lung injury in mice. , 2002, American journal of respiratory cell and molecular biology.

[33]  Y. Kan,et al.  Nrf2 is essential for protection against acute pulmonary injury in mice. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  D. Nebert,et al.  Possible Role of Cytochromes P450 in Lupus Erythematosus and Related Disorders , 1994, Lupus.

[35]  Y. ChanJ,et al.  酵母での遺伝的選択によるNF-E2関連転写因子、Nrf1のクローニング , 1993 .

[36]  J. Antonini,et al.  Superinduction of CYP1A1 Gene Expression , 2000, The Journal of Biological Chemistry.

[37]  Satoru Takahashi,et al.  EPR imaging of reducing activity in Nrf2 transcriptional factor-deficient mice. , 2003, Free radical biology & medicine.

[38]  Satoru Takahashi,et al.  Nrf2 regulates the sensitivity of death receptor signals by affecting intracellular glutathione levels , 2003, Oncogene.

[39]  Laura Leung,et al.  Deficiency of the Nrf1 and Nrf2 Transcription Factors Results in Early Embryonic Lethality and Severe Oxidative Stress* , 2003, Journal of Biological Chemistry.

[40]  Ning Li,et al.  Nrf2 Is a Key Transcription Factor That Regulates Antioxidant Defense in Macrophages and Epithelial Cells: Protecting against the Proinflammatory and Oxidizing Effects of Diesel Exhaust Chemicals1 , 2004, The Journal of Immunology.

[41]  R. Scott,et al.  Phagocytosis and clearance of apoptotic cells is mediated by MER , 2001, Nature.