Rosiglitazone rescues memory impairment in Alzheimer's transgenic mice: Mechanisms involving a reduced amyloid and tau pathology

Neuropsychopharmacology

Volumn 35, Issue 7, 2010, Pages 1593-1604

  Escribano, Luis ^a   Simón, Ana María ^a   Gimeno, Esther ^a   Cuadrado Tejedor, Mar ^a   De Maturana, Rakel López ^a   García Osta, Ana ^a   Ricobaraza, Ana ^a   Pérez Mediavilla, Alberto ^a   Río, Joaquín Del ^a   Frechilla, Diana ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Alzheimer's disease; Amyloid; Hippocampus; Memory; PPARg; Tau

Indexed keywords

AMYLOID PRECURSOR PROTEIN; ROSIGLITAZONE; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DISEASE MARKER; ENTORHINAL CORTEX; GENE OVEREXPRESSION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MEMORY DISORDER; MICROGLIA; MOUSE; NEURITE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RECOGNITION; SPATIAL MEMORY;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD36; CYCLOOXYGENASE 2; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; HYPOGLYCEMIC AGENTS; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NEUROPSYCHOLOGICAL TESTS; PEPTIDE FRAGMENTS; RECOGNITION (PSYCHOLOGY); TAU PROTEINS; THIAZOLIDINEDIONES;

EID: 77952423753     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2010.32     Document Type: Article

References (55)

1. ADAPT Research Group (2008). Cognitive function over time in the Alzheimer's Disease Anti-inflammatory Prevention Trial (ADAPT): results of a randomized, controlled trial of naproxen and celecoxib. Arch Neurology 65: 896-905.
2. Bayer TA, Wirths O, Majtenyi K, Hartmann T, Multhaup G, Beyreuther K et al (2001). Key factors in Alzheimer's disease: beta-amyloid precursor protein processing, metabolism and intraneuronal transport. Brain Pathol 11: 1-11.
3. Biessels GJ, Kappelle LJ (2005). Increased risk of Alzheimer's disease in Type II diabetes: insulin resistance of the brain or insulin-induced amyloid pathology? Biochem Soc Trans 33: 1041-1044.
4. Broadbent NJ, Squire LR, Clark RE (2004). Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci USA 101: 14515-14520.
5. Camacho IE, Serneels L, Spittaels K, Merchiers P, Dominguez D, De Strooper B (2004). Peroxisome-proliferator-activated receptor gamma induces a clearance mechanism for the amyloid-beta peptide. J Neurosci 24: 10908-10917.
6. Cancino GI, Toledo EM, Leal NR, Hernandez DE, Yevenes LF, Inestrosa NC et al (2008). STI571 prevents apoptosis, tau phosphorylation and behavioural impairments induced by Alzheimer's beta-amyloid deposits. Brain 131: 2425-2442.
7. d'Abramo C, Massone S, Zingg JM, Pizzuti A, Marambaud P, Dalla Piccola B et al (2005). Role of peroxisome proliferator-activated receptor gamma in amyloid precursor protein processing and amyloid beta-mediated cell death. Biochem J 391: 693-698.
8. d'Abramo C, Ricciarelli R, Pronzato MA, Davies P (2006). Troglitazone, a peroxisome proliferator-activated receptor-gamma agonist, decreases tau phosphorylation in CHOtau4R cells. J Neurochem 98: 1068-1077.
9. Edwards JP, Zhang X, Frauwirth KA, Mosser DM (2006). Biochemical and functional characterization of three activated macrophage populations. J Leukoc Biol 80: 1298-1307.
10. El Khoury J, Hickman SE, Thomas CA, Loike JD, Silverstein SC (1998). Microglia, scavenger receptors, and the pathogenesis of Alzheimer's disease. Neurobiol Aging 19: S81-S84.
11. Escribano L, Simon AM, Perez-Mediavilla A, Salazar-Colocho P, Del Rio J, Frechilla D (2009). Rosiglitazone reverses memory decline and hippocampal glucocorticoid receptor down-regulation in an Alzheimer's disease mouse model. Biochem Biophys Res Commun 379: 406-410.
12. Fan J, Donkin J, Wellington C (2009). Greasing the wheels of Abeta clearance in Alzheimer's disease: the role of lipids and apolipoprotein E. Biofactors 35: 239-248.
13. Gerlai R (2001). Behavioral tests of hippocampal function: simple paradigms complex problems. Behav Brain Res 125: 269-277.
14. Hardy J, Selkoe DJ (2002). The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-356.
15. Heneka MT, Sastre M, Dumitrescu-Ozimek L, Hanke A, Dewachter I, Kuiperi C et al (2005). Acute treatment with the PPARgamma agonist pioglitazone and ibuprofen reduces glial inflammation and Abeta1-42 levels in APPV717I transgenic mice. Brain 128: 1442-1453.
16. Hodgkinson CP, Ye S (2003). Microarray analysis of peroxisome proliferator-activated receptor-gamma induced changes in gene expression in macrophages. Biochem Biophys Res Commun 308: 505-510.
17. Holmes C, Cunningham C, Zotova E, Woolford J, Dean C, Kerr S et al (2009). Systemic inflammation and disease progression in Alzheimer disease. Neurology 73: 768-774.
18. int'Veld BA, Ruitenberg A, Hofman A, Launer LJ, van Duijn CM, Stijnen T et al (2001). Nonsteroidal antiinflammatory drugs and the risk of Alzheimer's disease. N Engl J Med 345: 1515-1521.
19. Iwata N, Tsubuki S, Takaki Y, Watanabe K, Sekiguchi M, Hosoki E et al (2000). Identification of the major Abeta1-42-degrading catabolic pathway in brain parenchyma: suppression leads to biochemical and pathological deposition. Nat Med 6: 143-150.
20. Jiang Q, Lee CY, Mandrekar S, Wilkinson B, Cramer P, Zelcer N et al (2008). ApoE promotes the proteolytic degradation of Abeta. Neuron 58: 681-693.
21. Kurochkin IV, Goto S (1994). Alzheimer's beta-amyloid peptide specifically interacts with and is degraded by insulin degrading enzyme. FEBS Lett 345: 33-37.
22. Landreth GE, Heneka MT (2001). Anti-inflammatory actions of peroxisome proliferator-activated receptor gamma agonists in Alzheimer's disease. Neurobiol Aging 22: 937-944.
23. Lehmann JM, Lenhard JM, Oliver BB, Ringold GM, Kliewer SA (1997). Peroxisome proliferator-activated receptors alpha and gamma are activated by indomethacin and other non-steroidal anti-inflammatory drugs. J Biol Chem 272: 3406-3410.
24. Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, Kliewer SA (1995). An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J Biol Chem 270: 12953-12956.
25. Leissring MA, Farris W, Chang AY, Walsh DM, Wu X, Sun X et al (2003). Enhanced proteolysis of beta-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron 40: 1087-1093.
26. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A et al (2006). A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440: 352-357.
27. Martin RM, Leonhardt H, Cardoso MC (2005). DNA labeling in living cells. Cytometry A 67: 45-52.
28. McKee AC, Kosik KS, Kowall NW (1991). Neuritic pathology and dementia in Alzheimer's disease. Ann Neurol 30: 156-165.
29. Meilandt WJ, Cisse M, Ho K, Wu T, Esposito LA, Scearce-Levie K et al (2009). Neprilysin overexpression inhibits plaque formation but fails to reduce pathogenic Abeta oligomers and associated cognitive deficits in human amyloid precursor protein trans-genic mice. J Neurosci 29: 1977-1986.
30. Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G et al (2000). High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synapto-toxicity without plaque formation. J Neurosci 20: 4050-4058.
31. Nicolakakis N, Aboulkassim T, Ongali B, Lecrux C, Fernandes P, Rosa-Neto P et al (2008). Complete rescue of cerebrovascular function in aged Alzheimer's disease transgenic mice by antioxidants and pioglitazone, a peroxisome proliferator-acti-vated receptor gamma agonist. J Neurosci 28: 9287-9296.
32. Pedersen WA, McMillan PJ, Kulstad JJ, Leverenz JB, Craft S, Haynatzki GR (2006). Rosiglitazone attenuates learning and memory deficits in Tg2576 Alzheimer mice. Exp Neurol 199: 265-273.
33. Risner ME, Saunders AM, Altman JF, Ormandy GC, Craft S, Foley IM et al (2006). Efficacy of rosiglitazone in a genetically defined population with mild-to-moderate Alzheimer's disease. Pharma-cogenomics J 6: 246-254.
34. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, Wu T et al (2007). Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 316: 750-754.
35. Sastre M, Dewachter I, Rossner S, Bogdanovic N, Rosen E, Borghgraef P et al (2006). Nonsteroidal anti-inflammatory drugs repress beta-secretase gene promoter activity by the activation of PPARgamma. Proc Natl Acad Sci USA 103: 443-448.
36. Schiapparelli L, Simon AM, Del Rio J, Frechilla D (2006). Opposing effects of AMPA and 5-HT1A receptor blockade on passive avoidance and object recognition performance: correlation with AMPA receptor subunit expression in rat hippocampus. Neuropharmacology 50: 897-907.
37. Selkoe DJ (1994). Alzheimer's disease: a central role for amyloid. J Neuropathol Exp Neurol 53: 438-447.
38. Selkoe DJ (2001). Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J Alzheimers Dis 3: 75-80.
39. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S (2006). Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49: 489-502.
40. Strum JC, Shehee R, Virley D, Richardson J, Mattie M, Selley P et al (2007). Rosiglitazone induces mitochondrial biogenesis in mouse brain. J Alzheimers Dis 11: 45-51.
41. Su JH, Cummings BJ, Cotman CW (1998). Plaque biogenesis in brain aging and Alzheimer's disease. II. Progressive transformation and developmental sequence of dystrophic neurites. Acta Neuropathol 96: 463-471.
42. Sundararajan S, Jiang Q, Heneka M, Landreth G (2006). PPARgamma as a therapeutic target in central nervous system diseases. Neurochem Int 49: 136-144.
43. Tanzi RE, Moir RD, Wagner SL (2004). Clearance of Alzheimer's Abeta peptide: the many roads to perdition. Neuron 43: 605-608.
44. Toledo EM, Inestrosa NC (2010). Activation of Wnt signaling by lithium and rosiglitazone reduced spatial memory impairment and neurodegeneration in brains of an APPswe/PSEN1DE9 mouse model of Alzheimer's disease. Mol Psychiatry 15: 272-285.
45. Van Dam D, De Deyn PP (2006). Drug discovery in dementia: the role of rodent models. Nat Rev Drug Discov 5: 956-970.
46. Vekrellis K, Ye Z, Qiu W Q, Walsh D, Hartley D, Chesneau V et al (2000). Neurons regulate extracellular levels of amyloid beta-protein via proteolysis by insulin-degrading enzyme. J Neurosci 20: 1657-1665.
47. Venneti S, Wiley CA, Kofler J (2009). Imaging microglial activation during neuroinflammation and Alzheimer's disease. J Neuroim-mune Pharmacol 4: 227-243.
48. Wahrle SE, Jiang H, Parsadanian M, Kim J, Li A, Knoten A et al (2008). Overexpression of ABCA1 reduces amyloid deposition in the PDAPP mouse model of Alzheimer disease. J Clin Invest 118: 671-682.
49. Watson GS, Cholerton BA, Reger MA, Baker LD, Plymate SR, Asthana S et al (2005). Preserved cognition in patients with early Alzheimer disease and amnestic mild cognitive impairment during treatment with rosiglitazone: a preliminary study. Am J Geriatr Psychiatry 13: 950-958.
50. Westerman MA, Cooper-Blacketer D, Mariash A, Kotilinek L, Kawarabayashi T, Younkin LH et al (2002). The relationship between Abeta and memory in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 22: 1858-1867. (Pubitemid 35386304)
51. Wirths O, Multhaup G, Bayer TA (2004). A modified beta-amyloid hypothesis: intraneuronal accumulation of the beta-amyloid peptideFthe first step of a fatal cascade. J Neurochem 91: 513-520.
52. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A et al (1996). RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 382: 685-691.
53. Yan Q, Zhang J, Liu H, Babu-Khan S, Vassar R, Biere AL et al (2003). Anti-inflammatory drug therapy alters beta-amyloid processing and deposition in an animal model of Alzheimer's disease. J Neurosci 23: 7504-7509.
54. Zhao X, Grotta J, Gonzales N, Aronowski J (2009). Hematoma resolution as a therapeutic target: the role of microglia/macrophages. Stroke 40: S92-S94.
55. Zipp F, Aktas O (2006). The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases. Trends Neurosci 29: 518-527.