Pharmacological manipulation of peroxisome proliferator-activated receptor γ (PPARγ) reveals a role for anti-oxidant protection in a model of Parkinson's disease

Experimental Neurology

Volumn 235, Issue 2, 2012, Pages 528-538

  Martin, Heather L ^a   Mounsey, Ross B ^a   Mustafa, Sarah ^a   Sathe, Kinnari ^a   Teismann, Peter ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

MPP +; MPTP; Neurodegeneration; Parkinson's disease; Peroxisome proliferator activated receptor

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 2 CHLORO 5 NITROBENZANILIDE; 3,4 DIHYDROXYPHENYLACETIC ACID; DOPAMINE; GLUTATHIONE TRANSFERASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; REACTIVE OXYGEN METABOLITE; ROSIGLITAZONE; SUPEROXIDE DISMUTASE;

ANTIOXIDANT ACTIVITY; ARTICLE; CELL LOSS; CELL STRAIN; CELL SURVIVAL; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC ACTIVITY; DRUG TARGETING; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL; NEUROPROTECTION; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; SUBSTANTIA NIGRA PARS COMPACTA; UPREGULATION;

ANILIDES; ANIMALS; ANTIOXIDANTS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; HUMANS; MALE; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PARKINSON DISEASE; PPAR GAMMA; THIAZOLIDINEDIONES;

EID: 84860365643     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.02.017     Document Type: Article

References (48)

1. Barak Y., Nelson M.C., Ong E.S., Jones Y.Z., Ruiz-Lozano P., Chien K.R., Koder A., Evans R.M. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol. Cell 1999, 4:585-595.
2. Bernardo A., Levi G., Minghetti L. Role of the peroxisome proliferator-activated receptor-gamma (PPAR-gamma) and its natural ligand 15-deoxy-Delta12, 14-prostaglandin J2 in the regulation of microglial functions. Eur. J. Neurosci. 2000, 12:2215-2223.
3. Breidert T., Callebert J., Heneka M.T., Landreth G., Launay J.M., Hirsch E.C. Protective action of the peroxisome proliferator-activated receptor-gamma agonist pioglitazone in a mouse model of Parkinson's disease. J. Neurochem. 2002, 82:615-624.
4. Carta A.R., Frau L., Pisanu A., Wardas J., Spiga S., Carboni E. Rosiglitazone decreases peroxisome proliferator receptor-gamma levels in microglia and inhibits TNF-alpha production: new evidences on neuroprotection in a progressive Parkinson's disease model. Neuroscience 2011, 194:250-261.
5. Chintharlapalli S., Papineni S., Baek S.J., Liu S., Safe S. 1,1-Bis(3'-indolyl)-1-(p-substituted phenyl)methanes are peroxisome proliferator-activated receptor gamma agonists but decrease HCT-116 colon cancer cell survival through receptor-independent activation of early growth response-1 and nonsteroidal anti-inflammatory drug-activated gene-1. Mol. Pharmacol. 2005, 68:1782-1792.
6. Dauer W., Przedborski S. Parkinson's disease: mechanisms and models. Neuron 2003, 39:889-909.
7. Davies G.F., Khandelwal R.L., Wu L., Juurlink B.H., Roesler W.J. Inhibition of phosphoenolpyruvate carboxykinase (PEPCK) gene expression by troglitazone: a peroxisome proliferator-activated receptor-gamma (PPARgamma)-independent, antioxidant-related mechanism. Biochem. Pharmacol. 2001, 62:1071-1079.
8. Dehmer T., Heneka M.T., Sastre M., Dichgans J., Schulz J.B. Protection by pioglitazone in the MPTP model of Parkinson's disease correlates with IkappaBalpha induction and block of NFkappaB and iNOS activation. J. Neurochem. 2004, 88:494-501.
9. Delerive P., Fruchart J.C., Staels B. Peroxisome proliferator-activated receptors in inflammation control. J. Endocrinol. 2001, 169:453-459.
10. Desvergne B., Wahli W. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr. Rev. 1999, 20:649-688.
11. Devchand P.R., Keller H., Peters J.M., Vazquez M., Gonzalez F.J., Wahli W. The PPARalpha-leukotriene B4 pathway to inflammation control. Nature 1996, 384:39-43.
12. Du J., Sun B., Chen K., Fan L., Wang Z. Antagonist of peroxisome proliferator-activated receptor gamma induces cerebellar amyloid-beta levels and motor dysfunction in APP/PS1 transgenic mice. Biochem. Biophys. Res. Commun. 2009, 384:357-361.
13. EMA/CHMP/586211/2010. Questions and answers on the suspension of rosiglitazone-containing medicines (Avandia, Avandamet and Avaglim). http://www.ema.europa.eu/docs/en_GB/document_library/Medicine_QA/2010/09/WC500097003.pdf.
14. Escribano L., Simon A.M., Perez-Mediavilla A., Salazar-Colocho P., Del Rio J., Frechilla D. Rosiglitazone reverses memory decline and hippocampal glucocorticoid receptor down-regulation in an Alzheimer's disease mouse model. Biochem. Biophys. Res. Commun. 2009, 379:406-410.
15. Feinstein D.L., Galea E., Gavrilyuk V., Brosnan C.F., Whitacre C.C., Dumitrescu-Ozimek L., Landreth G.E., Pershadsingh H.A., Weinberg G., Heneka M.T. Peroxisome proliferator-activated receptor-gamma agonists prevent experimental autoimmune encephalomyelitis. Ann. Neurol. 2002, 51:694-702.
16. Fornai F., Carri M.T., Ferri A., Paolucci E., Prisco S., Bernardi G., Rotilio G., Mercuri N.B. Resistance to striatal dopamine depletion induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mice expressing human mutant Cu, Zn superoxide dismutase. Neurosci. Lett. 2002, 325:124-128.
17. Fuenzalida K., Quintanilla R., Ramos P., Piderit D., Fuentealba R.A., Martinez G., Inestrosa N.C., Bronfman M. Peroxisome proliferator-activated receptor gamma up-regulates the Bcl-2 anti-apoptotic protein in neurons and induces mitochondrial stabilization and protection against oxidative stress and apoptosis. J. Biol. Chem. 2007, 282:37006-37015.
18. Girnun G.D., Domann F.E., Moore S.A., Robbins M.E. Identification of a functional peroxisome proliferator-activated receptor response element in the rat catalase promoter. Mol. Endocrinol. 2002, 16:2793-2801.
19. Glass C.K., Saijo K., Winner B., Marchetto M.C., Gage F.H. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934.
20. Hald A., Lotharius J. Oxidative stress and inflammation in Parkinson's disease: is there a causal link?. Exp. Neurol. 2005, 193:279-290.
21. Hayes J.D., Flanagan J.U., Jowsey I.R. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 2005, 45:51-88.
22. Jackson-Lewis V., Przedborski S. Protocol for the MPTP mouse model of Parkinson's disease. Nat. Protoc. 2007, 2:141-151.
23. Jackson-Lewis V., Jakowec M., Burke R.E., Przedborski S. Time course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurodegeneration 1995, 4:257-269.
24. Jenner P. Oxidative stress in Parkinson's disease. Ann. Neurol. 2003, 53(3):S26-36. discussion S36-8.
25. Jiang C., Ting A.T., Seed B. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 1998, 391:82-86.
26. + induced cytotoxicity via inhibition of mitochondrial dysfunction and ROS production. J. Neurol. Sci. 2007, 253:53-60.
27. Kiaei M., Kipiani K., Chen J., Calingasan N.Y., Beal M.F. Peroxisome proliferator-activated receptor-gamma agonist extends survival in transgenic mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 2005, 191:331-336.
28. Nicolakakis N., Aboulkassim T., Ongali B., Lecrux C., Fernandes P., Rosa-Neto P., Tong X.K., Hamel E. Complete rescue of cerebrovascular function in aged Alzheimer's disease transgenic mice by antioxidants and pioglitazone, a peroxisome proliferator-activated receptor gamma agonist. J. Neurosci. 2008, 28:9287-9296.
29. Niino M., Iwabuchi K., Kikuchi S., Ato M., Morohashi T., Ogata A., Tashiro K., Onoe K. Amelioration of experimental autoimmune encephalomyelitis in C57BL/6 mice by an agonist of peroxisome proliferator-activated receptor-gamma. J. Neuroimmunol. 2001, 116:40-48.
30. Nuber S., Petrasch-Parwez E., Winner B., Winkler J., von Horsten S., Schmidt T., Boy J., Kuhn M., Nguyen H.P., Teismann P., Schulz J.B., Neumann M., Pichler B.J., Reischl G., Holzmann C., Schmitt I., Bornemann A., Kuhn W., Zimmermann F., Servadio A., Riess O. Neurodegeneration and motor dysfunction in a conditional model of Parkinson's disease. J. Neurosci. 2008, 28:2471-2484.
31. Ou Z., Zhao X., Labiche L.A., Strong R., Grotta J.C., Herrmann O., Aronowski J. Neuronal expression of peroxisome proliferator-activated receptor-gamma (PPARgamma) and 15d-prostaglandin J2-mediated protection of brain after experimental cerebral ischemia in rat. Brain Res. 2006, 1096:196-203.
32. Park E.Y., Cho I.J., Kim S.G. Transactivation of the PPAR-responsive enhancer module in chemopreventive glutathione S-transferase gene by the peroxisome proliferator-activated receptor-gamma and retinoid X receptor heterodimer. Cancer Res. 2004, 64:3701-3713.
33. Quinn L.P., Crook B., Hows M.E., Vidgeon-Hart M., Chapman H., Upton N., Medhurst A.D., Virley D.J. The PPARgamma agonist pioglitazone is effective in the MPTP mouse model of Parkinson's disease through inhibition of monoamine oxidase B. Br. J. Pharmacol. 2008, 154:226-233.
34. Quintanilla R.A., Jin Y.N., Fuenzalida K., Bronfman M., Johnson G.V. Rosiglitazone treatment prevents mitochondrial dysfunction in mutant Huntingtin-expressing cells: possible role of peroxisome proliferator-activated receptor-gamma (PPARgamma) in the pathogenesis of Huntington disease. J. Biol. Chem. 2008, 283:25628-25637.
35. Raikwar H.P., Muthian G., Rajasingh J., Johnson C., Bright J.J. PPARgamma antagonists exacerbate neural antigen-specific Th1 response and experimental allergic encephalomyelitis. J. Neuroimmunol. 2005, 167:99-107.
36. Ricote M., Li A.C., Willson T.M., Kelly C.J., Glass C.K. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 1998, 391:79-82.
37. Schintu N., Frau L., Ibba M., Caboni P., Garau A., Carboni E., Carta A.R. PPAR-gamma-mediated neuroprotection in a chronic mouse model of Parkinson's disease. Eur. J. Neurosci. 2009, 29:954-963.
38. Smeyne M., Boyd J., Raviie Shepherd K., Jiao Y., Pond B.B., Hatler M., Wolf R., Henderson C., Smeyne R.J. GSTpi expression mediates dopaminergic neuron sensitivity in experimental parkinsonism. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:1977-1982.
39. Storer P.D., Xu J., Chavis J., Drew P.D. Peroxisome proliferator-activated receptor-gamma agonists inhibit the activation of microglia and astrocytes: implications for multiple sclerosis. J. Neuroimmunol. 2005, 161:113-122.
40. Teismann P., Tieu K., Choi D.K., Wu D.C., Naini A., Hunot S., Vila M., Jackson-Lewis V., Przedborski S. Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:5473-5478.
41. Thal S.C., Heinemann M., Luh C., Pieter D., Werner C., Engelhard K. Pioglitazone reduces secondary brain damage after experimental brain trauma by PPAR-gamma-independent mechanisms. J. Neurotrauma 2011, 28:983-993.
42. Wang X., Wang Z., Liu J.Z., Hu J.X., Chen H.L., Li W.L., Hai C.X. Double antioxidant activities of rosiglitazone against high glucose-induced oxidative stress in hepatocyte. Toxicol. In. Vitro. 2011, 25:839-847.
43. West M.J. New stereological methods for counting neurons. Neurobiol. Aging 1993, 14:275-285.
44. Wu D.C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D.K., Ischiropoulos H., Przedborski S. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 2002, 22:1763-1771.
45. Xiong H., Callaghan D., Jones A., Walker D.G., Lue L.F., Beach T.G., Sue L.I., Woulfe J., Xu H., Stanimirovic D.B., Zhang W. Cholesterol retention in Alzheimer's brain is responsible for high beta- and gamma-secretase activities and Abeta production. Neurobiol. Dis. 2008, 29:422-437.
46. Yoo H.Y., Chang M.S., Rho H.M. Induction of the rat Cu/Zn superoxide dismutase gene through the peroxisome proliferator-responsive element by arachidonic acid. Gene 1999, 234:87-91.
47. Zhao X., Strong R., Zhang J., Sun G., Tsien J.Z., Cui Z., Grotta J.C., Aronowski J. Neuronal PPARgamma deficiency increases susceptibility to brain damage after cerebral ischemia. J. Neurosci. 2009, 29:6186-6195.
48. Zorov D.B., Juhaszova M., Yaniv Y., Nuss H.B., Wang S., Sollott S.J. Regulation and pharmacology of the mitochondrial permeability transition pore. Cardiovasc. Res. 2009, 83:213-225.