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PMID: 10995830 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Peroxisome proliferator-activated receptor-gamma ligands reduce neuronal inducible nitric oxide synthase expression and cell death in vivo.

Heneka MT, Klockgether T, Feinstein DL

Abstract

Expression of the inducible form of nitric oxide synthase (iNOS) in brain may contribute to neurotoxicity in Alzheimer's disease (AD). Expression of iNOS can be induced in cerebellar granule cells (CGCs) in vivo as well as in vitro, allowing these cells to be used to study regulation of neuronal iNOS expression. We report here that microinjection of bacterial lipopolysaccharide and interferon gamma into rat cerebellum induced iNOS expression in CGCs and subsequent cell death assessed by staining for DNA fragmentation. Co-injection of three structurally distinct agonists of the peroxisome proliferator-activated receptor gamma (PPARgamma), including the antidiabetic thiazolidinedione troglitazone, the nonsteroidal anti-inflammatory drug (NSAID) ibuprofen, and the prostanoid 15-deoxy-Delta(12,14) prostaglandin J(2), reduced both iNOS expression and cell death, whereas co-injection of the selective cyclo-oxygenase inhibitor NS-398 had no effect. These data demonstrate that PPARgamma agonists can modulate inflammatory responses in brain. Because sustained medication with NSAIDs reduces the risk and delays the onset of AD, these results further suggest that NSAIDs provide therapeutic value by binding to PPARgamma present in AD brain, thereby preventing iNOS expression and neuronal cell death.

MeSH Terms
Animals Anti-Inflammatory Agents, Non-Steroidal/administration & dosage,metabolism Cell Death/drug effects Cerebellum/drug effects,metabolism Chromans/administration & dosage,metabolism Cyclooxygenase Inhibitors/administration & dosage,metabolism Down-Regulation/drug effects Ibuprofen/administration & dosage,metabolism Immunohistochemistry In Situ Nick-End Labeling Interferon-gamma/administration & dosage Ligands Lipopolysaccharides/administration & dosage Male Microinjections Nitric Oxide Synthase/biosynthesis Nitric Oxide Synthase Type II Nitrobenzenes/administration & dosage Prostaglandin D2/administration & dosage,analogs & derivatives,metabolism Rats Rats, Sprague-Dawley Receptors, Cytoplasmic and Nuclear/metabolism Sulfonamides/administration & dosage Thiazoles/administration & dosage,metabolism Thiazolidinediones Transcription Factors/metabolism Troglitazone
Chemicals
15-deoxy-delta(12,14)-prostaglandin J2 Anti-Inflammatory Agents, Non-Steroidal Chromans Cyclooxygenase Inhibitors Ligands Lipopolysaccharides Nitrobenzenes Receptors, Cytoplasmic and Nuclear Sulfonamides Thiazoles Thiazolidinediones Transcription Factors N-(2-cyclohexyloxy-4-nitrophenyl)methanesulfonamide Interferon-gamma Nitric Oxide Synthase Nitric Oxide Synthase Type II Nos2 protein, rat Troglitazone Prostaglandin D2 Ibuprofen
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Heneka M T
Department of Neurology, University of Bonn, 53105 Bonn, Germany. [email protected]
Klockgether T
Feinstein D L
References (43)
43 references, click to expand
  1. Inducible nitric oxide synthase in tangle-bearing neurons of patients with Alzheimer's disease.
    J Exp Med. 1996 Oct 1;184(4):1425-33 PMID: 8879214
  2. Peroxisome proliferator-activated receptors: a nuclear receptor signaling pathway in lipid physiology.
    Annu Rev Cell Dev Biol. 1996;12:335-63 PMID: 8970730
  3. Increased expression of cyclooxygenases and peroxisome proliferator-activated receptor-gamma in Alzheimer's disease brains.
    Biochem Biophys Res Commun. 1999 Jan 27;254(3):582-6 PMID: 9920782
  4. Widespread peroxynitrite-mediated damage in Alzheimer's disease.
    J Neurosci. 1997 Apr 15;17(8):2653-7 PMID: 9092586
  5. Nitric oxide synthase induces macrophage death by apoptosis.
    Biochem Biophys Res Commun. 1993 Mar 15;191(2):503-8 PMID: 7681667
  6. Activation of human T lymphocytes is inhibited by peroxisome proliferator-activated receptor gamma (PPARgamma) agonists. PPARgamma co-association with transcription factor NFAT.
    J Biol Chem. 2000 Feb 18;275(7):4541-4 PMID: 10671476
  7. Peroxisome proliferator-activated receptor gamma agonists protect cerebellar granule cells from cytokine-induced apoptotic cell death by inhibition of inducible nitric oxide synthase.
    J Neuroimmunol. 1999 Dec;100(1-2):156-68 PMID: 10695726
  8. Risk of Alzheimer's disease and duration of NSAID use.
    Neurology. 1997 Mar;48(3):626-32 PMID: 9065537
  9. Induction of calcium-independent nitric oxide synthase activity in cultured cerebellar granule neurons.
    Neurosci Lett. 1995 Jan 23;184(2):145-8 PMID: 7536905
  10. Inhibition of NF-kappaB potentiates amyloid beta-mediated neuronal apoptosis.
    Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9409-14 PMID: 10430956
  11. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  12. A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor gamma and promotes adipocyte differentiation.
    Cell. 1995 Dec 1;83(5):813-9 PMID: 8521498
  13. Medical significance of peroxisome proliferator-activated receptors.
    Lancet. 1999 Jul 10;354(9173):141-8 PMID: 10408502
  14. Interferon-gamma plus lipopolysaccharide induction of delayed neuronal apoptosis in rat hippocampus.
    Neurochem Int. 1999 Feb;34(2):91-9 PMID: 10213066
  15. Activation of peroxisome proliferator-activated receptor gamma does not inhibit IL-6 or TNF-alpha responses of macrophages to lipopolysaccharide in vitro or in vivo.
    J Immunol. 2000 Jan 15;164(2):1046-54 PMID: 10623855
  16. Inhibition of inducible nitric oxide synthase by peroxisome proliferator-activated receptor agonists: correlation with induction of heme oxygenase 1.
    J Immunol. 1998 Jul 15;161(2):978-84 PMID: 9670978
  17. PPAR tissue distribution and interactions with other hormone-signaling pathways.
    Ann N Y Acad Sci. 1996 Dec 27;804:231-51 PMID: 8993547
  18. Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha, -beta, and -gamma in the adult rat.
    Endocrinology. 1996 Jan;137(1):354-66 PMID: 8536636
  19. Troglitazone, a new antidiabetic agent possessing radical scavenging ability, improved decreased skin blood flow in diabetic rats.
    Life Sci. 1998;63(22):2039-47 PMID: 9839548
  20. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation.
    Nature. 1998 Jan 1;391(6662):79-82 PMID: 9422508
  21. Inflammatory mechanisms in Alzheimer's disease: implications for therapy.
    Am J Psychiatry. 1994 Aug;151(8):1105-13 PMID: 7518651
  22. Chronic overexpression of proinflammatory cytokines and histopathology in the brains of rats infected with Trypanosoma brucei.
    J Comp Neurol. 1999 Nov 8;414(1):114-30 PMID: 10494082
  23. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines.
    Nature. 1998 Jan 1;391(6662):82-6 PMID: 9422509
  24. Arthritis and anti-inflammatory agents as possible protective factors for Alzheimer's disease: a review of 17 epidemiologic studies.
    Neurology. 1996 Aug;47(2):425-32 PMID: 8757015
  25. Peroxisome proliferator-activated receptors alpha and gamma are activated by indomethacin and other non-steroidal anti-inflammatory drugs.
    J Biol Chem. 1997 Feb 7;272(6):3406-10 PMID: 9013583
  26. S100 beta induces apoptotic cell death in cultured astrocytes via a nitric oxide-dependent pathway.
    Biochim Biophys Acta. 1996 Oct 11;1313(3):239-45 PMID: 8898860
  27. Inducible nitric oxide synthase immunoreactivity in the Alzheimer disease hippocampus: association with Hirano bodies, neurofibrillary tangles, and senile plaques.
    J Neuropathol Exp Neurol. 1999 Nov;58(11):1163-9 PMID: 10560659
  28. Delayed onset of Alzheimer's disease with nonsteroidal anti-inflammatory and histamine H2 blocking drugs.
    Neurobiol Aging. 1995 Jul-Aug;16(4):523-30 PMID: 8544901
  29. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IkappaB kinase.
    Nature. 2000 Jan 6;403(6765):103-8 PMID: 10638762
  30. 15-Deoxy-delta 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR gamma.
    Cell. 1995 Dec 1;83(5):803-12 PMID: 8521497
  31. The PPARs: from orphan receptors to drug discovery.
    J Med Chem. 2000 Feb 24;43(4):527-50 PMID: 10691680
  32. The heat shock response inhibits NF-kappaB activation, nitric oxide synthase type 2 expression, and macrophage/microglial activation in brain.
    J Cereb Blood Flow Metab. 2000 May;20(5):800-11 PMID: 10826530
  33. Expression of inducible nitric oxide synthase causes delayed neurotoxicity in primary mixed neuronal-glial cortical cultures.
    Neuropharmacology. 1994 Nov;33(11):1425-30 PMID: 7532825
  34. Activators of peroxisome proliferator-activated receptor-gamma (PPARgamma) inhibit inducible nitric oxide synthase expression but increase heme oxygenase-1 expression in rat glial cells.
    Neurosci Lett. 1999 Mar 5;262(2):129-32 PMID: 10203248
  35. Toxicity of human THP-1 monocytic cells towards neuron-like cells is reduced by non-steroidal anti-inflammatory drugs (NSAIDs).
    Neuropharmacology. 1999 Jul;38(7):1017-25 PMID: 10428420
  36. Induction of nitric oxide synthase and nitric oxide-mediated apoptosis in neuronal PC12 cells after stimulation with tumor necrosis factor-alpha/lipopolysaccharide.
    J Neurochem. 1998 Jul;71(1):88-94 PMID: 9648854
  37. Inflammatory mechanisms in Alzheimer's disease: inhibition of beta-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARgamma agonists.
    J Neurosci. 2000 Jan 15;20(2):558-67 PMID: 10632585
  38. Inflammatory mediator stimulation of astrocytes and meningeal fibroblasts induces neuronal degeneration via the nitridergic pathway.
    J Neurochem. 1995 Jan;64(1):266-76 PMID: 7798922
  39. Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight.
    J Neurosci Methods. 1985 Apr;13(2):139-43 PMID: 3889509
  40. The peroxisome proliferator-activated receptor(PPARgamma) as a regulator of monocyte/macrophage function.
    J Leukoc Biol. 1999 Nov;66(5):733-9 PMID: 10577502
  41. In vivo expression of inducible nitric oxide synthase in cerebellar neurons.
    J Neurochem. 1996 Apr;66(4):1504-9 PMID: 8627305
  42. Beta-amyloid binds to p57NTR and activates NFkappaB in human neuroblastoma cells.
    J Neurosci Res. 1998 Dec 15;54(6):798-804 PMID: 9856863
  43. Cyclopentenone prostaglandins suppress activation of microglia: down-regulation of inducible nitric-oxide synthase by 15-deoxy-Delta12,14-prostaglandin J2.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4668-73 PMID: 10200320
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
2000-09-15
Pages
6862-7
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6772804
Subset
IM
Grants
NINDS NIH HHS · NS-31556 · United States
Corrections
ErratumIn
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