A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death.
paper
Cited
Public
- Authors
- Saijo, Kaoru; Winner, Beate; Carson, Christian T; Collier, Jana G; Boyer, Leah; Rosenfeld, Michael G; Gage, Fred H; Glass, Christopher K
- Year
- 2009
- Journal
- Cell
- PMID
- 19345186
- DOI
- 10.1016/j.cell.2009.01.038
- PMCID
- PMC2754279
Nurr1, an orphan nuclear receptor, plays an essential role in the generation and maintenance of dopaminergic neurons in the brain. Rare mutations in Nurr1 are associated with familial Parkinson's disease, but the underlying basis for this relationship has not been established. Here, we demonstrate that Nurr1 unexpectedly functions to inhibit expression of pro-inflammatory neurotoxic mediators in both microglia and astrocytes. Reduced Nurr1 expression results in exaggerated inflammatory responses in microglia that are further amplified by astrocytes, leading to the production of factors that cause death of tyrosine hydroxylase-expressing neurons. Nurr1 exerts anti-inflammatory effects by docking to NF-kappaB-p65 on target inflammatory gene promoters in a signal-dependent manner. Subsequently, Nurr1 recruits the CoREST corepressor complex, resulting in clearance of NF-kappaB-p65 and transcriptional repression. These studies suggest that Nurr1 protects against loss of dopaminergic neurons in Parkinson's disease in part by limiting the production of neurotoxic mediators by microglia and astrocytes.
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| 40 | Experimental Procedures β RNA isolation and quantitative PCR | Total RNA was isolated by RNAeasy kit (Qiagen) from cells or SN samples microdissected from theβ¦ |
| 41 | Experimental Procedures β Statistical analyses | Standard deviation, Chi-square and two-tail Studentβs t-test were performed with the Prism 4β¦ |
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| Activation of the astrocytic Nrf2/ARE system ameliorates the formation of demyelinating lesions in a multiple sclerosis animal model. | Draheim T et al. | β | 2016 | β |
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| Daphnane Diterpenes from Daphne genkwa Activate Nurr1 and Have a Neuroprotective Effect in an Animal Model of Parkinson's Disease. | Han BS et al. | β | 2016 | β |
| Dual and Opposing Roles of MicroRNA-124 in Epilepsy Are Mediated through Inflammatory and NRSF-Dependent Gene Networks. | Brennan GP et al. | β | 2016 | β |
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| Gas1 up-regulation is inducible and contributes to cell apoptosis in reactive astrocytes in the substantia nigra of LPS and MPTP models. | Sun XL et al. | β | 2016 | β |
| Genome Wide Mapping of NR4A Binding Reveals Cooperativity with ETS Factors to Promote Epigenetic Activation of Distal Enhancers in Acute Myeloid Leukemia Cells. | Duren RP et al. | β | 2016 | β |
| Heterogeneous astrocytes: Active players in CNS. | Hu X et al. | β | 2016 | β |
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| Nuclear receptor 4A (NR4A) family - orphans no more. | Safe S et al. | β | 2016 | β |
| Nurr1 and PPARΞ³ protect PC12 cells against MPP(+) toxicity: involvement of selective genes, anti-inflammatory, ROS generation, and antimitochondrial impairment. | Jodeiri Farshbaf M et al. | β | 2016 | β |
| Nurr1-Based Therapies for Parkinson's Disease. | Dong J et al. | β | 2016 | β |
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| Ontogeny of Tumor-associated Macrophages and Its Implication in Cancer Regulation. | Franklin RA et al. | β | 2016 | β |
| Opposite effects of acute and chronic amphetamine on Nurr1 and NF-ΞΊB p65 in the rat ventral tegmental area. | Arredondo C et al. | β | 2016 | β |
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| Protein kinase CΞ΄ upregulation in microglia drives neuroinflammatory responses and dopaminergic neurodegeneration in experimental models of Parkinson's disease. | Gordon R et al. | β | 2016 | β |
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| Upregulation of Glutaredoxin-1 Activates Microglia and Promotes Neurodegeneration: Implications for Parkinson's Disease. | Gorelenkova Miller O et al. | β | 2016 | β |
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| ALS Patient Stem Cells for Unveiling Disease Signatures of Motoneuron Susceptibility: Perspectives on the Deadly Mitochondria, ER Stress and Calcium Triad. | Kaus A et al. | β | 2015 | β |
| Amyloid-Ξ² reduces the expression of neuronal FAIM-L, thereby shifting the inflammatory response mediated by TNFΞ± from neuronal protection to death. | Carriba P et al. | β | 2015 | β |
| A novel synthetic activator of Nurr1 induces dopaminergic gene expression and protects against 6-hydroxydopamine neurotoxicity in vitro. | Hammond SL et al. | β | 2015 | β |
| A Nurr1 agonist causes neuroprotection in a Parkinson's disease lesion model primed with the toll-like receptor 3 dsRNA inflammatory stimulant poly(I:C). | Smith GA et al. | β | 2015 | β |
| Brain iron accumulation exacerbates the pathogenesis of MPTP-induced Parkinson's disease. | You LH et al. | β | 2015 | β |
| Chronic Toxoplasma gondii in Nurr1-null heterozygous mice exacerbates elevated open field activity. | Eells JB et al. | β | 2015 | β |
| Combined Nurr1 and Foxa2 roles in the therapy of Parkinson's disease. | Oh SM et al. | β | 2015 | β |
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| Lipoic acid protects dopaminergic neurons in LPS-induced Parkinson's disease model. | Li YH et al. | β | 2015 | β |
| Molecular Interactions between NR4A Orphan Nuclear Receptors and NF-ΞΊB Are Required for Appropriate Inflammatory Responses and Immune Cell Homeostasis. | Murphy EP et al. | β | 2015 | β |
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| NOR-1 modulates the inflammatory response of vascular smooth muscle cells by preventing NFΞΊB activation. | Calvayrac O et al. | β | 2015 | β |
| Novel para-phenyl substituted diindolylmethanes protect against MPTP neurotoxicity and suppress glial activation in a mouse model of Parkinson's disease. | De Miranda BR et al. | β | 2015 | β |
| NR4A receptors up-regulate the antiproteinase alpha-2 macroglobulin (A2M) and modulate MMP-2 and MMP-9 in vascular smooth muscle cells. | RodrΓguez-Calvo R et al. | β | 2015 | β |
| Nuclear Receptor Nr4a2 Promotes Alternative Polarization of Macrophages and Confers Protection in Sepsis. | Mahajan S et al. | β | 2015 | β |
| Nuclear receptor Nurr1 agonists enhance its dual functions and improve behavioral deficits in an animal model of Parkinson's disease. | Kim CH et al. | β | 2015 | β |
| NURR1 involvement in recombinant tissue-type plasminogen activator treatment complications after ischemic stroke. | Merino-Zamorano C et al. | β | 2015 | β |
| Nurr1 reduction influences the onset of chronic EAE in mice. | Montarolo F et al. | β | 2015 | β |
| PDLIM1 inhibits NF-ΞΊB-mediated inflammatory signaling by sequestering the p65 subunit of NF-ΞΊB in the cytoplasm. | Ono R et al. | β | 2015 | β |
| PRDX6 Exacerbates Dopaminergic Neurodegeneration in a MPTP Mouse Model of Parkinson's Disease. | Yun HM et al. | β | 2015 | β |
| Redox regulation of NF-ΞΊB p50 and M1 polarization in microglia. | Taetzsch T et al. | β | 2015 | β |
| Retinoic acid-loaded polymeric nanoparticles induce neuroprotection in a mouse model for Parkinson's disease. | Esteves M et al. | β | 2015 | β |
| Role of autophagy in the pathogenesis of multiple sclerosis. | Liang P et al. | β | 2015 | β |
| Secreted miR-34a in astrocytic shedding vesicles enhanced the vulnerability of dopaminergic neurons to neurotoxins by targeting Bcl-2. | Mao S et al. | β | 2015 | β |
| Sulfhydryl-mediated redox signaling in inflammation: role in neurodegenerative diseases. | Gorelenkova Miller O et al. | β | 2015 | β |
| Suppression of Th2 and Tfh immune reactions by Nr4a receptors in mature T reg cells. | Sekiya T et al. | β | 2015 | β |
| TAM receptor deficiency affects adult hippocampal neurogenesis. | Ji R et al. | β | 2015 | β |
| The association between infectious burden and Parkinson's disease: A case-control study. | Bu XL et al. | β | 2015 | β |
| The choreography of neuroinflammation in Huntington's disease. | Crotti A et al. | β | 2015 | β |
| The glucocorticoid mometasone furoate is a novel FXR ligand that decreases inflammatory but not metabolic gene expression. | Bijsmans IT et al. | β | 2015 | β |
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| The NR4A orphan nuclear receptors: mediators in metabolism and diseases. | Ranhotra HS | β | 2015 | β |
| The nuclear receptor nr4a1 controls CD8 T cell development through transcriptional suppression of runx3. | Nowyhed HN et al. | β | 2015 | β |
| The Nurr1 Activator 1,1-Bis(3'-Indolyl)-1-(p-Chlorophenyl)Methane Blocks Inflammatory Gene Expression in BV-2 Microglial Cells by Inhibiting Nuclear Factor ΞΊB. | De Miranda BR et al. | β | 2015 | β |
| Transcription factor myocyte enhancer factor 2D regulates interleukin-10 production in microglia to protect neuronal cells from inflammation-induced death. | Yang S et al. | β | 2015 | β |
| Transcription factor Nr4a1 couples sympathetic and inflammatory cues in CNS-recruited macrophages to limit neuroinflammation. | Shaked I et al. | β | 2015 | β |
| A20 deficiency causes spontaneous neuroinflammation in mice. | Guedes RP et al. | β | 2014 | β |
| Activated astrocytes enhance the dopaminergic differentiation of stem cells and promote brain repair through bFGF. | Yang F et al. | β | 2014 | β |
| A genome-wide linkage scan of bipolar disorder in Latino families identifies susceptibility loci at 8q24 and 14q32. | Gonzalez S et al. | β | 2014 | β |
| Amyloid Beta, TNFΞ± and FAIM-L; Approaching New Therapeutic Strategies for AD. | Carriba P et al. | β | 2014 | β |
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| A survey from 2012 of evidence for the role of neuroinflammation in neurotoxin animal models of Parkinson's disease and potential molecular targets. | Ramsey CP et al. | β | 2014 | β |
| Biological role of Toll-like receptor-4 in the brain. | Trotta T et al. | β | 2014 | β |
| Can we switch microglia's phenotype to foster neuroprotection? Focus on multiple sclerosis. | Giunti D et al. | β | 2014 | β |
| Deficiency of the NR4A orphan nuclear receptor NOR1 in hematopoietic stem cells accelerates atherosclerosis. | Qing H et al. | β | 2014 | β |
| Differential properties of transcriptional complexes formed by the CoREST family. | Barrios ΓP et al. | β | 2014 | β |
| Early miR-155 upregulation contributes to neuroinflammation in Alzheimer's disease triple transgenic mouse model. | Guedes JR et al. | β | 2014 | β |
| Effects of isoxazolo-pyridinone 7e, a potent activator of the Nurr1 signaling pathway, on experimental autoimmune encephalomyelitis in mice. | Montarolo F et al. | β | 2014 | β |
| Eryptosis as a marker of Parkinson's disease. | Pretorius E et al. | β | 2014 | β |
| Foxa2 acts as a co-activator potentiating expression of the Nurr1-induced DA phenotype via epigenetic regulation. | Yi SH et al. | β | 2014 | β |
| Functional crosstalk of PGC-1 coactivators and inflammation in skeletal muscle pathophysiology. | Eisele PS et al. | β | 2014 | β |
| Glia in the pathogenesis of neurodegenerative diseases. | Verkhratsky A et al. | β | 2014 | β |
| Glial modulators as potential treatments of psychostimulant abuse. | Beardsley PM et al. | β | 2014 | β |
| Herbal medicines for ischemic stroke: combating inflammation as therapeutic targets. | Gu Y et al. | β | 2014 | β |
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| Inflammasomes: molecular regulation and implications for metabolic and cognitive diseases. | Choi AJ et al. | β | 2014 | β |
| Inhibition of Methicillin-resistant Staphylococcus aureus-induced cytokines mRNA production in human bone marrow derived mesenchymal stem cells by 1,25-dihydroxyvitamin D3. | Maiti A et al. | β | 2014 | β |
| Jmjd3 is essential for the epigenetic modulation of microglia phenotypes in the immune pathogenesis of Parkinson's disease. | Tang Y et al. | β | 2014 | β |
| KrΓΌppel-like factor 6 is a co-activator of NF-ΞΊB that mediates p65-dependent transcription of selected downstream genes. | Zhang Y et al. | β | 2014 | β |
| LIN28 expression in rat spinal cord after injury. | Yue Y et al. | β | 2014 | β |
| Maternal immune activation and abnormal brain development across CNS disorders. | Knuesel I et al. | β | 2014 | β |
| MC1R and NR4A receptors in cellular stress and DNA repair: implications for UVR protection. | Yin K et al. | β | 2014 | β |
| Microglia dictate the impact of saturated fat consumption on hypothalamic inflammation and neuronal function. | Valdearcos M et al. | β | 2014 | β |
| Microglia in Alzheimer's disease. | Li Y et al. | β | 2014 | β |
| Microglial activation mediates host neuronal survival induced by neural stem cells. | Wu HM et al. | β | 2014 | β |
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| Microglia: unique and common features with other tissue macrophages. | Prinz M et al. | β | 2014 | β |
| Molecular mechanisms linking neuroinflammation and neurodegeneration in MS. | Ellwardt E et al. | β | 2014 | β |
| Monocytes and CD4+ T cells contribution to the under-expression of NR4A2 and TNFAIP3 genes in patients with multiple sclerosis. | Navone ND et al. | β | 2014 | β |
| Murine dopaminergic MΓΌller cells restore motor function in a model of Parkinson's disease. | Stutz B et al. | β | 2014 | β |
| Mutant Huntingtin promotes autonomous microglia activation via myeloid lineage-determining factors. | Crotti A et al. | β | 2014 | β |
| NR4A nuclear receptors are orphans but not lonesome. | Kurakula K et al. | β | 2014 | β |
| Nuclear receptors in neurodegenerative diseases. | Skerrett R et al. | β | 2014 | β |
| Nurr1 expression is regulated by voltage-dependent calcium channels and calcineurin in cultured hippocampal neurons. | Tokuoka H et al. | β | 2014 | β |
| Paroxetine ameliorates lipopolysaccharide-induced microglia activation via differential regulation of MAPK signaling. | Liu RP et al. | β | 2014 | β |
| Rcor2 underexpression in senescent mice: a target for inflammaging? | Alvarez-LΓ³pez MJ et al. | β | 2014 | β |
| Regulation of caspase-3 processing by cIAP2 controls the switch between pro-inflammatory activation and cell death in microglia. | Kavanagh E et al. | β | 2014 | β |
| Suppression of Alzheimer-associated inflammation by microglial prostaglandin-E2 EP4 receptor signaling. | Woodling NS et al. | β | 2014 | β |
| Systemic regulation of mammalian ageing and longevity by brain sirtuins. | Satoh A et al. | β | 2014 | β |
| The NR4A receptors Nurr1 and Nur77 are increased in human placenta from women with gestational diabetes. | Lappas M | β | 2014 | β |
| The nuclear receptor Nr4a1 mediates anti-inflammatory effects of apoptotic cells. | Ipseiz N et al. | β | 2014 | β |
| Yin and yang of tumor inflammation: how innate immune suppressors shape the tumor microenvironments. | Jinushi M | β | 2014 | β |
| Ξ²-arrestin protects neurons by mediating endogenous opioid arrest of inflammatory microglia. | Feng X et al. | β | 2014 | β |
| Adult neurogenesis in Parkinson's disease. | Marxreiter F et al. | β | 2013 | β |
| Analysis of the RelA:CBP/p300 interaction reveals its involvement in NF-ΞΊB-driven transcription. | Mukherjee SP et al. | β | 2013 | β |
| Anti-neuroinflammatory agents for the treatment of Alzheimer's disease. | Zhou W et al. | β | 2013 | β |
| Bone marrow NR4A expression is not a dominant factor in the development of atherosclerosis or macrophage polarization in mice. | Chao LC et al. | β | 2013 | β |
| Ca(2+) spiking activity caused by the activation of store-operated Ca(2+) channels mediates TNF-Ξ± release from microglial cells under chronic purinergic stimulation. | Ikeda M et al. | β | 2013 | β |
| Cellular and molecular mediators of neuroinflammation in the pathogenesis of Parkinson's disease. | More SV et al. | β | 2013 | β |
| Cytosolic phospholipase A(2)Ξ± and eicosanoids regulate expression of genes in macrophages involved in host defense and inflammation. | Suram S et al. | β | 2013 | β |
| Depletion of microglia from primary cellular cultures. | Pont-Lezica L et al. | β | 2013 | β |
| Development and homeostasis of "resident" myeloid cells: the case of the microglia. | Gomez Perdiguero E et al. | β | 2013 | β |
| Dual effects of peroxisome proliferator-activated receptor Ξ³ on embryonic stem cell self-renewal in presence and absence of leukemia inhibitory factor. | Peymani M et al. | β | 2013 | β |
| Early life permethrin exposure induces long-term brain changes in Nurr1, NF-kB and Nrf-2. | Carloni M et al. | β | 2013 | β |
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| Exosomes of BV-2 cells induced by alpha-synuclein: important mediator of neurodegeneration in PD. | Chang C et al. | β | 2013 | β |
| Glial-mediated inflammation underlying parkinsonism. | Barcia C | β | 2013 | β |
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| Nuclear import and export signals control the subcellular localization of Nurr1 protein in response to oxidative stress. | GarcΓa-YagΓΌe ΓJ et al. | β | 2013 | β |
| Nuclear orphan receptor NR4A2 confers chemoresistance and predicts unfavorable prognosis of colorectal carcinoma patients who received postoperative chemotherapy. | Han Y et al. | β | 2013 | β |
| Nuclear receptor NR4A2 orchestrates Th17 cell-mediated autoimmune inflammation via IL-21 signalling. | Raveney BJ et al. | β | 2013 | β |
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| O-GlcNAc transferase inhibits LPS-mediated expression of inducible nitric oxide synthase through an increased interaction with mSin3A in RAW264.7 cells. | Hwang SY et al. | β | 2013 | β |
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