Autoradiographical imaging of PPARγ agonist effects on PBR/TSPO binding in TASTPM mice

Experimental Neurology

Volumn 216, Issue 2, 2009, Pages 459-470

  Roberts, Jennifer C ^a   Friel, Sarah L ^a   Roman, Shilina ^a   Perren, Marion ^a   Harper, Alex ^a   Davis, John B ^a   Richardson, Jill C ^a   Virley, David ^a   Medhurst, Andrew D ^a  

^a GLAXOSMITHKLINE   (United Kingdom)

Author keywords

3H (R) PK11195; 3H DPA 713; Autoradiography; Ciglitazone; Microglia; Peripheral benzodiazepine receptor; Pioglitazone; TASTPM mice; Translocator protein (18 kDa)

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BENZODIAZEPINE RECEPTOR; CARRIER PROTEIN; CD68 ANTIGEN; CIGLITAZONE; DPA 713; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; PIOGLITAZONE; PRESENILIN 1; RADIOLIGAND; TRITIUM; UNCLASSIFIED DRUG; 2,4 THIAZOLIDINEDIONE DERIVATIVE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; ACETAMIDE DERIVATIVE; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); CD68 ANTIGEN, HUMAN; DIFFERENTIATION ANTIGEN; ISOQUINOLINE DERIVATIVE; LEUKOCYTE ANTIGEN; N,N DIETHYL 2 (2 (4 METHOXYPHENYL) 5,7 DIMETHYL PYRAZOLO(1,5 A)PYRIMIDIN 3 YL) ACETAMIDE; N,N-DIETHYL-2-(2-(4-METHOXYPHENYL)-5,7-DIMETHYL-PYRAZOLO(1,5-A)PYRIMIDIN-3-YL)-ACETAMIDE; PEPTIDE FRAGMENT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; TSPO PROTEIN, HUMAN;

AGED; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; AUTORADIOGRAPHY; BRAIN CORTEX; CELL ACTIVATION; CONTROLLED STUDY; DRUG EFFECT; EX VIVO STUDY; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SENILE PLAQUE; TRANSGENIC MOUSE; WILD TYPE; AGE; ANIMAL; BRAIN MAPPING; DRUG POTENTIATION; GENETICS; GLIA; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN BINDING; TIME;

ACETAMIDES; AGE FACTORS; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; AUTORADIOGRAPHY; BRAIN MAPPING; CEREBRAL CORTEX; FEMALE; HUMANS; ISOQUINOLINES; MALE; MICE; MICE, TRANSGENIC; NEUROGLIA; PEPTIDE FRAGMENTS; PPAR GAMMA; PRESENILIN-1; PROTEIN BINDING; PYRAZOLES; PYRIMIDINES; RECEPTORS, GABA; RECEPTORS, GABA-A; THIAZOLIDINEDIONES; TIME FACTORS;

EID: 62049083382     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.01.002     Document Type: Article

References (56)

1. Akiyama H., Barger S., Barnum S., Bradt B., Bauer J., Cole G.M., Cooper N.R., Eikelenboom P., Emmerling M., Fiebich B.L., Finch C.E., Frautschy S., Griffin W.S., Hampel H., Hull M., Landreth G., Lue L., Mrak R., Mackenzie I.R., McGeer P.L., O'Banion M.K., Pachter J., Pasinetti G., Plata-Salaman C., Rogers J., Rydel R., Shen Y., Streit W., Strohmeyer R., Tooyoma I., Van Muiswinkel F.L., Veerhuis R., Walker D., Webster S., Wegrzyniak B., Wenk G., and Wyss-Coray T. Inflammation and Alzheimer's disease. Neurobiol. Aging 21 (2000) 383-421
2. Anholt R.R., Pedersen P.L., De Souza E.B., and Snyder S.H. The peripheral-type benzodiazepine receptor. Localization to the mitochondrial outer membrane. J. Biol. Chem. 261 (1986) 576-583
3. Banati R.B. Visualising microglial activation in vivo. Glia 40 (2002) 206-217
4. Bauer J., Strauss S., Schreiter-Gasser U., Ganter U., Schlegel P., Witt I., Yolk B., and Berger M. Interleukin-6 and alpha-2-macroglobulin indicate an acute-phase state in Alzheimer's disease cortices. FEBS Lett. 285 (1991) 111-114
5. Benzing W.C., Wujek J.R., Ward E.K., Shaffer D., Ashe K.H., Younkin S.G., and Brunden K.R. Evidence for glial-mediated inflammation in aged APP(SW) transgenic mice. Neurobiol. Aging 20 (1999) 581-589
6. Bornemann K.D., Wiederhold K.H., Pauli C., Ermini F., Stalder M., Schnell L., Sommer B., Jucker M., and Staufenbiel M. Abeta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am. J. Pathol. 158 (2001) 63-73
7. Boutin H., Chauveau F., Thominiaux C., Gregoire M.C., James M.L., Trebossen R., Hantraye P., Dolle F., Tavitian B., and Kassiou M. 11C-DPA-713: a novel peripheral benzodiazepine receptor PET ligand for in vivo imaging of neuroinflammation. J. Nucl. Med. 48 (2007) 573-581
8. Braak H., and Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82 (1991) 239-259
9. Breitner J.C., Welsh K.A., Helms M.J., Gaskell P.C., Gau B.A., Roses A.D., Pericak-Vance M.A., and Saunders A.M. Delayed onset of Alzheimer's disease with nonsteroidal anti-inflammatory and histamine H2 blocking drugs. Neurobiol. Aging 16 (1995) 523-530
10. Cagnin A., Brooks D.J., Kennedy A.M., Gunn R.N., Myers R., Turkheimer F.E., Jones T., and Banati R.B. In-vivo measurement of activated microglia in dementia. Lancet 358 (2001) 461-467
11. Cagnin A., Kassiou M., Meikle S.R., and Banati R.B. Positron emission tomography imaging of neuroinflammation. Neurotherapeutics 4 (2007) 443-452
12. Casellas P., Galiegue S., and Basile A.S. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem. Int. 40 (2002) 475-486
13. Cumming P., Pedersen M.D., Minuzzi L., Mezzomo K., Danielsen E.H., Iversen P., Aagaard D., Keiding S., Munk O.L., and Finsen B. Distribution of PK11195 binding sites in porcine brain studied by autoradiography in vitro and by positron emission tomography. Synapse 59 (2006) 418-426
14. Daynes R.A., and Jones D.C. Emerging roles of PPARs in inflammation and immunity. Nat. Rev., Immunol. 2 (2002) 748-759
15. Diorio D., Welner S.A., Butterworth R.F., Meaney M.J., and Suranyi-Cadotte B.E. Peripheral benzodiazepine binding sites in Alzheimer's disease frontal and temporal cortex. Neurobiol. Aging 12 (1991) 255-258
16. Frautschy S.A., Yang F., Irrizarry M., Hyman B., Saido T.C., Hsiao K., and Cole G.M. Microglial response to amyloid plaques in APPsw transgenic mice. Am. J. Pathol. 152 (1998) 307-317
17. Griffin W.S., Stanley L.C., Ling C., White L., MacLeod V., Perrot L.J., White III C.L., and Araoz C. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 7611-7615
18. Heneka M.T., Klockgether T., and Feinstein D.L. Peroxisome proliferator-activated receptor-gamma ligands reduce neuronal inducible nitric oxide synthase expression and cell death in vivo. J. Neurosci. 20 (2000) 6862-6867
19. Heneka M.T., Sastre M., Dumitrescu-Ozimek L., Hanke A., Dewachter I., Kuiperi C., O'Banion K., Klockgether T., Van Leuven F., and Landreth G.E. Acute treatment with the PPARgamma agonist pioglitazone and ibuprofen reduces glial inflammation and Abeta1-42 levels in APPV717I transgenic mice. Brain 128 (2005) 1442-1453
20. Highman B. Improved methods for demonstrating amyloid in paraffin sections. Arch. Pathol. 41 (1946) 559
21. Howlett D.R., Richardson J.C., Austin A., Parsons A.A., Bate S.T., Davies D.C., and Gonzalez M.I. Cognitive correlates of Abeta deposition in male and female mice bearing amyloid precursor protein and presenilin-1 mutant transgenes. Brain Res. 1017 (2004) 130-136
22. Howlett D.R., Bowler K., Soden P.E., Riddell D., Davis J.B., Richardson J.C., Burbidge S.A., Gonzalez M.I., Irving E.A., Lawman A., Miglio G., Dawson E.L., Howlett E.R., and Hussain I. Abeta deposition and related pathology in an APP × PS1 transgenic mouse model of Alzheimer's disease. Histol. Histopathol. 23 (2008) 67-76
23. James M.L., Fulton R.R., Henderson D.J., Eberl S., Meikle S.R., Thomson S., Allan R.D., Dolle F., Fulham M.J., and Kassiou M. Synthesis and in vivo evaluation of a novel peripheral benzodiazepine receptor PET radioligand. Bioorg. Med. Chem. 13 (2005) 6188-6194
24. Jiang C., Ting A.T., and Seed B. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 391 (1998) 82-86
25. Kapadia R., Yi J.H., and Vemuganti R. Mechanisms of anti-inflammatory and neuroprotective actions of PPAR-gamma agonists. Front. Biosci. 13 (2008) 1813-1826
26. Kielian T., Syed M.M., Liu S., Phulwani N.K., Phillips N., Wagoner G., Drew P.D., and Esen N. The synthetic peroxisome proliferator-activated receptor-gamma agonist ciglitazone attenuates neuroinflammation and accelerates encapsulation in bacterial brain abscesses. J. Immunol. 180 (2008) 5004-5016
27. Kubota N., Terauchi Y., Kubota T., Kumagai H., Itoh S., Satoh H., Yano W., Ogata H., Tokuyama K., Takamoto I., Mineyama T., Ishikawa M., Moroi M., Sugi K., Yamauchi T., Ueki K., Tobe K., Noda T., Nagai R., and Kadowaki T. Pioglitazone ameliorates insulin resistance and diabetes by both adiponectin-dependent and -independent pathways. J. Biol. Chem. 281 (2006) 8748-8755
28. Landreth G. Therapeutic use of agonists of the nuclear receptor PPARgamma in Alzheimer's disease. Curr. Alzheimer Res. 4 (2007) 159-164
29. Le Fur G., Vaucher N., Perrier M.L., Flamier A., Benavides J., Renault C., Dubroeucq M.C., Gueremy C., and Uzan A. Differentiation between two ligands for peripheral benzodiazepine binding sites, [3H]RO5-4864 and [3H]PK 11195, by thermodynamic studies. Life Sci. 33 (1983) 449-457
30. Lehmann J.M., Lenhard J.M., Oliver B.B., Ringold G.M., and Kliewer S.A. Peroxisome proliferator-activated receptors α and γ are activated by indomethacin and other non-steroidal anti-inflammatory drugs. J. Biol. Chem. 272 (1997) 3406-3410
31. Lim G.P., Yang F., Chu T., Chen P., Beech W., Teter B., Tran T., Ubeda O., Ashe K.H., Frautschy S.A., and Cole G.M. Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J. Neurosci. 20 (2000) 5709-5714
32. Matsuoka Y., Picciano M., Malester B., LaFrancois J., Zehr C., Daeschner J.M., Olschowka J.A., Fonseca M.I., O'Banion M.K., Tenner A.J., Lemere C.A., and Duff K. Inflammatory responses to amyloidosis in a transgenic mouse model of Alzheimer's disease. Am. J. Pathol. 158 (2001) 1345-1354
33. McGeer P.L., and McGeer E.G. Mechanisms of cell death in Alzheimer disease-immunopathology. J. Neural Transm., Suppl. 54 (1998) 159-166
34. Mittelbronn M., Dietz K., Schluesener H.J., and Meyermann R. Local distribution of microglia in the normal adult central nervous system differs by up to one order of magnitude. Acta Neuropathol. 101 (2001) 249-255
35. Papadopoulos V. Peripheral-type benzodiazepine receptor in neurosteroid biosynthesis, neuropathology and neurological disorders. Neuroscience 138 (2006) 749-756
36. Papadopoulos V., Baraldi M., Guilarte T.R., Knudsen T.B., Lacapère J.-J., Lindemann P., Norenberg M.D., Nutt D., Weizman A., Zhang M.-R., and Gavish M. Translocator protein (18 kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol. Sci. 27 (2006) 402-409
37. Pedersen M.D., Minuzzi L., Wirenfeldt M., Meldgaard M., Slidsborg C., Cumming P., and Finsen B. Up-regulation of PK11195 binding in areas of axonal degeneration coincides with early microglial activation in mouse brain. Eur. J. Neurosci. 24 (2006) 991-1000
38. Pedersen W.A., McMillan P.J., Kulstad J.J., Leverenz J.B., Craft S., and Haynatzki G.R. Rosiglitazone attenuates learning and memory deficits in Tg2576 Alzheimer mice. Exp. Neurol. 199 (2006) 265-273
39. Raghavendra Rao V.L., Dogan A., Bowen K.K., and Dempsey R.J. Traumatic brain injury leads to increased expression of peripheral-type benzodiazepine receptors, neuronal death, and activation of astrocytes and microglia in rat thalamus. Exp. Neurol. 161 (2000) 102-114
40. Richardson J.C., Kendal C.E., Anderson R., Priest F., Gower E., Soden P., Gray R., Topps S., Howlett D.R., Lavender D., Clarke N.J., Barnes J.C., Haworth R., Stewart M.G., and Rupniak H.T. Ultrastructural and behavioural changes precede amyloid deposition in a transgenic model of Alzheimer's disease. Neuroscience 122 (2003) 213-228
41. Roberts J.C., Davis J.B., and Benham C.D. [3H]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res. 995 (2004) 176-183
42. 3H]PK11195 and real time autoradiography. 8th International conference on Alzheimer's Disease and Parkinson's Disease (ADPD), Salzburg, Austria.
43. Rogers J., Webster S., Lue L.F., Brachova L., Civin W.H., Emmerling M., Shivers B., Walker D., and McGeer P. Inflammation and Alzheimer's disease pathogenesis. Neurobiol. Aging 17 (1996) 681-686
44. Rosario E.R., Chang L., Stanczyk F.Z., and Pike C.J. Age-related testosterone depletion and the development of Alzheimer Disease. JAMA 292 (2004) 1431-1432
45. Schwab C., Hosokawa M., and McGeer P.L. Transgenic mice overexpressing amyloid beta protein are an incomplete model of Alzheimer disease. Exp. Neurol. 188 (2004) 52-64
46. Selleri S., Bruni F., Costagli C., Costanzo A., Guerrini G., Ciciani G., Costa B., and Martini C. 2-Arylpyrazolo[1,5-a]pyrimidin-3-yl acetamides. New potent and selective peripheral benzodiazepine receptor ligands. Bioorg. Med. Chem. 9 (2001) 2661-2671
47. Stalder M., Phinney A., Probst A., Sommer B., Staufenbiel M., and Jucker M. Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am. J. Pathol. 154 (1999) 1673-1684
48. Stephenson D.T., Schober D.A., Smalstig E.B., Mincy R.E., Gehlert D.R., and Clemens J.A. Peripheral benzodiazepine receptors are colocalized with activated microglia following transient global forebrain ischemia in the rat. J. Neurosci. 15 (1995) 5263-5274
49. Stewart W.F., Kawas C., Corrada M., and Metter E.J. Risk of Alzheimer's disease and duration of NSAID use. Neurology 48 (1997) 626-632
50. Vela J.M., Dalmau I., Gonzalez B., and Castellano B. Morphology and distribution of microglial cells in the young and adult mouse cerebellum. J. Comp. Neurol. 361 (1995) 602-616
51. Venneti S., Lopresti B.J., Wang G., Bissel S.J., Mathis C.A., Meltzer C.C., Boada F., Capuano III S., Kress G.J., Davis D.K., Ruszkiewicz J., Reynolds I.J., Murphey-Corb M., Trichel A.M., Wisniewski S.R., and Wiley C.A. PET imaging of brain macrophages using the peripheral benzodiazepine receptor in a macaque model of neuroAIDS. J. Clin. Invest. 113 (2004) 981-989
52. Venneti S., Lopresti B.J., Wang G., Slagel S.L., Mason N.S., Mathis C.A., Fischer M.L., Larsen N.J., Mortimer A.D., Hastings T.G., Smith A.D., Zigmond M.J., Suhara T., Higuchi M., and Wiley C.A. A comparison of the high-affinity peripheral benzodiazepine receptor ligands DAA1106 and (R)-PK11195 in rat models of neuroinflammation: implications for PET imaging of microglial activation. J. Neurochem. 102 (2007) 2118-2131
53. Venneti S., Lopresti B.J., Wang G., Hamilton R.L., Mathis C.A., Klunk W.E., Apte U.M., and Wiley C.A. PK11195 labels activated microglia in Alzheimer's disease and in vivo in a mouse model using PET. Neurobiol. Aging (2008) 10.1016/jneurobiolaging.2007.11.005
54. Vlad S.C., Miller D.R., Kowell N.W., and Felson D.T. Protective effects of NSAIDS on the development of Alzheimer Disease. Neurology 70 (2008) 1672-1677
55. Wyss-Coray T., and Mucke L. Inflammation in neurodegenerative disease-a double-edged sword. Neuron 35 (2002) 419-432
56. Yan Q., Zhang J., Liu H., Babu-Khan S., Vassar R., Biere A.L., Citron M., and Landreth G. Anti-inflammatory drug therapy alters beta-amyloid processing and deposition in an animal model of Alzheimer's disease. J. Neurosci. 23 (2003) 7504-7509