Acute treatment with the PPARγ agonist pioglitazone and ibuprofen reduces glial inflammation and Aβ1-42 levels in APPV717I transgenic mice

Brain

Volumn 128, Issue 6, 2005, Pages 1442-1453

  Heneka, Michael T ^a,e   Sastre, Magdalena ^a   Dumitrescu Ozimek, Lucia ^a   Hanke, Anne ^a   Dewachter, Ilse ^b   Kuiperi, Cuno ^b   O'Banion, Kerry ^c   Klockgether, Thomas ^a   Van Leuven, Fred ^b   Landreth, Gary E ^d  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Alzheimer's disease; Inflammation; Neurodegeneration; NSAID; PPAR

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; BETA SECRETASE 1; CYCLOOXYGENASE 2; IBUPROFEN; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; NONSTEROID ANTIINFLAMMATORY AGENT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; UNCLASSIFIED DRUG; 2,4 THIAZOLIDINEDIONE DERIVATIVE; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); ASPARTIC PROTEINASE; BACE1 PROTEIN, MOUSE; GLIAL FIBRILLARY ACIDIC PROTEIN; NITRIC OXIDE SYNTHASE; NOS2 PROTEIN, MOUSE; PEPTIDE FRAGMENT; PROSTAGLANDIN SYNTHASE; PROTEINASE; SECRETASE;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DRUG MECHANISM; DRUG RECEPTOR BINDING; HIPPOCAMPUS; INFLAMMATION; MICROGLIA; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RECEPTOR UPREGULATION; TRANSGENIC MOUSE; ANIMAL; DISEASE MODEL; DRUG EFFECT; DRUG POTENTIATION; ENZYME IMMUNOASSAY; GENETICS; METABOLISM; PATHOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID PRECURSOR PROTEIN SECRETASES; AMYLOIDOSIS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ASPARTIC ENDOPEPTIDASES; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; ENDOPEPTIDASES; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; IBUPROFEN; IMMUNOENZYME TECHNIQUES; MICE; MICE, TRANSGENIC; MICROGLIA; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PEPTIDE FRAGMENTS; PPAR GAMMA; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RNA, MESSENGER; THIAZOLIDINEDIONES;

EID: 20444499367     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/awh452     Document Type: Article

References (72)

1. Aisen PS. Evaluation of selective COX-2 inhibitors for the treatment of Alzheimer's disease. J Pain Symptom Manag 2002; 23: S35-40.
2. Aisen PS, Schafer KA, Grundman M, et al. Effects of rofecoxib or naproxen vs placebo on Alzheimer disease progression: a randomized controlled trial. J Am Med Assoc 2003; 289: 2819-26.
3. Akiyama H, Barger S, Barnum S, et al. Inflammation and Alzheimer's disease. Neurobiol Aging 2000; 21: 383-421.
4. Alafuzoff I, Overmyer M, Helisalmi S, Soininen H. Lower counts of astroglia and activated microglia in patients with Alzheimer's disease with regular use of non-steroidal anti-inflammatory drugs. J Alzheimers Dis 2000; 2: 37-46.
5. Bannwarth B, Lapicque F, Pehourcq F, et al. Stereoselective disposition of ibuprofen enantiomers in human cerebrospinal fluid. Br J Clin Pharmacol 1995; 40: 266-9.
6. Bannwarth B, Netter P, Pourel J, Royer RJ, Gaucher A. Clinical pharmacokinetics of nonsteroidal anti-inflammatory drugs in the cerebrospinal fluid. Biomed Pharmacother 1989; 43: 121-6.
7. Barelli H, Lebeau A, Vizzavona J, et al. Characterization of new polyclonal antibodies specific for 40 and 42 amino acid-long amyloid beta peptides: their use to examine the cell biology of presenilins and the immunohistochemistry of sporadic Alzheimer's disease and cerebral amyloid angiopathy cases. Mol Med 1997; 3: 695-707.
8. Benzing WC, Wujek JR, Ward EK, et al. Evidence for glial-mediated inflammation in aged APP(SW) transgenic mice. Neurobiol Aging 1999; 20: 581-9.
9. Blasko I, Apochal A, Boeck G, Hartmann T, Grubeck-Loebenstein B, Ransmayr G. Ibuprofen decreases cytokine-induced amyloid beta production in neuronal cells. Neurobiol Dis 2001; 8: 1094-101.
10. Bondolfi L, Calhoun M, Ermini F, et al. Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice. J Neurosci 2002; 22: 515-22.
11. Bornemann KD, Wiederhold KH, Pauli C, et al. Abeta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am J Pathol 2001; 158: 63-73.
12. Breidert T, Callebert J, Heneka MT, Landreth G, Launay JM, Hirsch EC. Protective action of the peroxisome proliferator-activated receptor-gamma agonist pioglitazone in a mouse model of Parkinson's disease. J Neurochem 2002; 82: 615-24.
13. Chawla A, Barak Y, Nagy L, Liao D, Tontonoz P, Evans RM. PPAR-gamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat Med 2001; 7: 48-52.
14. Combs CK, Johnson DE, Karlo JC, Cannady SB, Landreth GE. Inflammatory mechanisms in Alzheimer's disease: inhibition of beta-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARgamma agonists. J Neurosci 2000; 20: 558-67.
15. Daynes RA, Jones DC. Emerging roles of PPARs in inflammation and immunity. Nat Rev Immunol 2002; 2: 748-59.
16. Diab A, Deng C, Smith JD, et al. Peroxisome proliferator-activated receptor-gamma agonist 15-deoxy-Delta(12,14)-prostaglandin J(2) ameliorates experimental autoimmune encephalomyelitis. J Immunol 2002; 168: 2508-15.
17. Dingwall C. Spotlight on BACE: the secretases as targets for treatment in Alzheimer disease. J Clin Invest 2001; 108: 1243-6.
18. Eriksen JL, Sagi SA, Smith TE, et al. NSAIDs and enantiomers of flurbiprofen target gamma-secretase and lower Abeta 42 in vivo. J Clin Invest 2003; 112: 440-9.
19. Esler WP, Wolfe MS. A portrait of Alzheimer secretases-new features and familiar faces. Science 2001; 293: 1449-54.
20. Feinstein DL, Galea E, Gavrilyuk V, et al. Peroxisome proliferator-activated receptor-gamma agonists prevent experimental autoimmune encephalomyelitis. Ann Neurol 2002; 51: 694-702.
21. Frautschy SA, Yang F, Irrizarry M, et al. Microglial response to amyloid plaques in APPsw transgenic mice. Am J Pathol 1998; 152: 307-17.
22. Griffin WS, Sheng JG, Royston MC, et al. Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathol 1998; 8: 65-72.
23. Hardy J, Allsop D. Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 1991; 12: 383-8.
24. Heneka MT, Feinstein DL, Galea E, Gleichmann M, Wullner U, Klockgether T. 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; 100: 156-68.
25. Heneka MT, Klockgether T, Feinstein DL. Peroxisome proliferator-activated receptor-gamma ligands reduce neuronal inducible nitric oxide synthase expression and cell death in vivo. J Neurosci 2000; 20: 6862-7.
26. Heneka MT, Galea E, Gavriluyk V, et al. Noradrenergic depletion potentiates beta-amyloid-induced cortical inflammation: implications for Alzheimer's disease. J Neurosci 2002; 22: 2434-42.
27. Ho L, Qin W, Pompl PN, et al. Diet-induced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer's disease. FASEB J 2004; 18: 902-4.
28. Hsiao KK, Borchelt DR, Olson K, et al. Age-related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins. Neuron 1995; 15: 1203-18.
29. Hurley SD, Olschowka JA, O'Banion MK. Cyclooxygenase inhibition as a strategy to ameliorate brain injury. J Neurotrauma 2002; 19: 1-15.
30. Iadecola C, Niwa K, Nogawa S, et al. Reduced susceptibility to ischemic brain injury and N-methyl-D-aspartate-mediated neurotoxicity in cyclooxygenase-2-deficient mice. Proc Natl Acad Sci USA 2001; 98: 1294-9.
31. In t'Veld, Ruitenberg A, Hofman A, et al. Nonsteroidal antiinflammatory drugs and the risk of Alzheimer's disease. N Engl J Med 2001; 345: 1515-21.
32. Jantzen PT, Connor KE, DiCarlo G, et al. Microglial activation and beta-amyloid deposit reduction caused by a nitric oxide-releasing nonsteroidal anti-inflammatory drug in amyloid precursor protein plus presenilin-1 transgenic mice. J Neurosci 2002; 22: 2246-54.
33. Jaradat MS, Wongsud B, Phornchirasilp S, et al. Activation of peroxisome proliferator-activated receptor isoforms and inhibition of prostaglandin H(2) synthases by ibuprofen, naproxen, and indomethacin. Biochem Pharmacol 2001; 62: 1587-95.
34. Jiang C, Ting AT, Seed B. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 1998; 391: 82-6.
35. Kojo H, Fukagawa M, Tajima K, et al. Evaluation of human peroxisome proliferator-activated receptor (PPAR) subtype selectivity of a variety of anti-inflammatory drugs based on a novel assay for PPAR delta(beta). J Pharmacol Sci 2003; 93: 347-55.
36. Lamb BT, Bardel KA, Kulnane LS, et al. Amyloid production and deposition in mutant amyloid precursor protein and presenilin-1 yeast artificial chromosome transgenic mice. Nat Neurosci 1999; 2: 695-7.
37. Landreth GE, Heneka MT. Anti-inflammatory actions of peroxisome proliferator-activated receptor gamma agonists in Alzheimer's disease. Neurobiol Aging 2001; 22: 937-44.
38. Lehmann JM, Lenhard JM, Oliver BB, Ringold GM, Kliewer SA. Peroxisome proliferator-activated receptors alpha and gamma are activated by indomethacin and other non-steroidal anti-inflammatory drugs. J Biol Chem 1997; 272: 3406-10.
39. Lim GP, Yang F, Chu T, et al. Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J Neurosci 2000; 20: 5709-14.
40. Lim GP, Yang F, Chu T, et al. Ibuprofen effects on Alzheimer pathology and open field activity in APPsw transgenic mice. Neurobiol Aging 2001; 22: 983-91.
41. Mackenzie IR, Munoz DG. Nonsteroidal anti-inflammatory drug use and Alzheimer-type pathology in aging. Neurology 1998; 50: 986-90.
42. Maeshiba Y, Kiyota Y, Yamashita K, Yoshimura Y, Motohashi M, Tanayama S. Disposition of the new antidiabetic agent pioglitazone in rats, dogs, and monkeys. Arzneimittel-Forschung 1997; 47: 29-35.
43. Manabe Y, Anrather J, Kawano T, et al. Prostanoids, not reactive oxygen species, mediate COX-2-dependent neurotoxicity. Ann Neurol 2004; 55: 668-75.
44. Matsuoka Y, Picciano M, Malester B, et al. Inflammatory responses to amyloidosis in a transgenic mouse model of Alzheimer's disease. Am J Pathol 2001; 158: 1345-54.
45. McGeer PL, Schulzer M, McGeer EG. Arthritis and anti-inflammatory agents as possible protective factors for Alzheimer's disease: a review of 17 epidemiologic studies. Neurology 1996; 47: 425-32.
46. Mehlhorn G, Hollborn M, Schliebs R. Induction of cytokines in glial cells surrounding cortical beta-amyloid plaques in transgenic Tg2576 mice with Alzheimer pathology. Int J Dev Neurosci 2000; 18: 423-31.
47. Moechars D, Dewachter I, Lorent K, et al. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J Biol Chem 1999; 274: 6483-92.
48. Montine TJ, Sidell KR, Crews BC, et al. Elevated CSF prostaglandin E2 levels in patients with probable AD. Neurology 1999; 53: 1495-8.
49. Natarajan C, Bright JJ. Peroxisome proliferator-activated receptor-gamma agonists inhibit experimental allergic encephalomyelitis by blocking IL-12 production, IL-12 signaling and Th1 differentiation. Genes Immun 2002; 3: 59-70.
50. Naujoks-Manteuffel C, Niemann U. Microglial cells in the brain of Pleurodeles waltl (Urodela, Salamandridae) after wallerian degeneration in the primary visual system using Bandeiraea simplicifolia isolectin B4-cytochemistry. Glia 1994; 10: 101-13.
51. Niino M, Iwabuchi K, Kikuchi S, et al. Amelioration of experimental autoimmune encephalomyelitis in C57BL/6 mice by an agonist of peroxisome proliferator-activated receptor-gamma. J Neuroimmunol 2001; 116: 40-8.
52. Parmentier-Batteur S, Bohme GA, Lerouet D, et al. Antisense oligodeoxy-nucleotide to inducible nitric oxide synthase protects against transient focal cerebral ischemia-induced brain injury. J Cereb Blood Flow Metab 2001; 21: 15-21.
53. Patsouris D, Muller M, Kersten S. Peroxisome proliferator activated receptor ligands for the treatment of insulin resistance. Curr Opin Invest Drugs 2004; 5: 1045-50.
54. Pompl PN, Ho L, Bianchi M, McManus T, Qin W, Pasinetti GM. A therapeutic role for cyclooxygenase-2 inhibitors in a transgenic mouse model of amyotrophic lateral sclerosis. FASEB J 2003; 17: 725-7.
55. Quinn J, Montine T, Morrow J, Woodward WR, Kulhanek D, Eckenstein F. Inflammation and cerebral amyloidosis are disconnected in an animal model of Alzheimer's disease. J Neuroimmunol 2003; 137: 32-41.
56. Ricote M, Li AC, Willson TM, Kelly CJ, Glass CK. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 1998; 391: 79-82.
57. Sagi SA, Weggen S, Eriksen J, Golde TE, Koo EH. The non-cyclooxygenase targets of non-steroidal anti-inflammatory drugs, lipoxygenases, peroxisome proliferator-activated receptor, inhibitor of kappa B kinase, and NF kappa B, do not reduce amyloid beta 42 production. J Biol Chem 2003; 278: 31825-30.
58. Sastre M, Dewachter I, Landreth GE, et al. Nonsteroidal anti-inflammatory drugs and peroxisome proliferator-activated receptor-gamma agonists modulate immunostimulated processing of amyloid precursor protein through regulation of beta-secretase. J Neurosci 2003; 23: 9796-804.
59. Shiomi T, Tsutsui H, Hayashidani S, et al. Pioglitazone, a peroxisome proliferator-activated receptor-gamma agonist, attenuates left ventricular remodeling and failure after experimental myocardial infarction. Circulation 2002; 106: 3126-32.
60. Stalder M, Phinney A, Probst A, Sommer B, Staufenbiel M, Jucker M. Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am J Pathol 1999; 154: 1673-84.
61. Stewart WF, Kawas C, Corrada M, Metter EJ. Risk of Alzheimer's disease and duration of NSAID use. Neurology 1997; 48: 626-32.
62. Sturchler-Pierrat C, Abramowski D, Duke M, et al. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci USA 1997; 94: 13287-92.
63. Tegeder I, Pfeilschifter J, Geisslinger G. Cyclooxygenase-independent actions of cyclooxygenase inhibitors. FASEB J 2001; 15: 2057-72.
64. Van Dorpe J, Smeijers L, Dewachter I, et al. Prominent cerebral amyloid angiopathy in transgenic mice overexpressing the London mutant of human APP in neurons. Am J Pathol 2000; 157: 1283-98.
65. Van Leuven F. Single and multiple transgenic mice as models for Alzheimer's disease. Prog Neurobiol 2000; 61: 305-12.
66. Watson GS, Craft S. The role of insulin resistance in the pathogenesis of Alzheimer's disease: implications for treatment. CNS Drugs 2003; 17: 27-45.
67. Weggen S, Eriksen JL, Das P, et al. A subset of NSAIDs lower amyloidogenic Abeta42 independently of cyclooxygenase activity. Nature 2001; 414: 212-6.
68. Wyss-Coray T, Mucke L. Inflammation in neurodegenerative disease-a double-edged sword. Neuron 2002; 35: 419-42.
69. Xiang Z, Ho L, Yemul S, et al. Cyclooxygenase-2 promotes amyloid plaque deposition in a mouse model of Alzheimer's disease neuropathology. Gene Expr2002; 10: 271-8.
70. Van Q, Zhang J, Liu H, et al. Anti-inflammatory drug therapy alters beta-amyloid processing and deposition in an animal model of Alzheimer's disease. J Neurosci 2003; 23: 7504-9.
71. Yki-Jarvinen H. Thiazolidinediones. N Engl J Med 2004; 351: 1106-18.
72. Zhang F, Casey RM, Ross ME, Iadecola C. Aminoguanidine ameliorates and L-arginine worsens brain damage from intraluminal middle cerebral artery occlusion. Stroke 1996; 27: 317-23.