Imaging of peripheral benzodiazepine receptor expression as biomarkers of detrimental versus beneficial glial responses in mouse models of Alzheimer's and other CNS pathologies

Journal of Neuroscience

Volumn 28, Issue 47, 2008, Pages 12255-12267

  Ji, Bin ^a   Maeda, Jun ^a   Sawada, Makoto ^b   Ono, Maiko ^a   Okauchi, Takashi ^a   Inaji, Motoki ^a   Zhang, Ming Rong ^a   Suzuki, Kazutoshi ^a   Ando, Kiyoshi ^a,c   Staufenbiel, Matthias ^d   Trojanowski, John Q ^e   Lee, Virginia M Y ^e   Higuchi, Makoto ^a   Suhara, Tetsuya ^a  

^a NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c CENTRAL INSTITUTE FOR EXPERIMENTAL ANIMALS   (Japan)

^d NOVARTIS PHARMA AG   (Switzerland)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Alzheimer's disease; Astrocyte; Glial cell line derived neurotrophic factor; Microglia; Neurodegenerative disorders; Peripheral benzodiazepine receptor

Indexed keywords

AMYLOID BETA PROTEIN; BENZODIAZEPINE RECEPTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; DISEASE MARKER; DOPAMINERGIC ACTIVITY; FEMALE; GLIA; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR DYNAMICS; MOUSE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

ACETAMIDES; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANALYSIS OF VARIANCE; ANIMALS; CELL LINE, TRANSFORMED; CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; KAINIC ACID; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; NEUROTOXICITY SYNDROMES; OXIDOPAMINE; PHENYL ETHERS; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; RATS; RECEPTORS, GABA-A; SENILE PLAQUES; TAU PROTEINS;

EID: 58149391968     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2312-08.2008     Document Type: Article

References (69)

1. Ando K, Maeda J, Inaji M, Okauchi T, Obayashi S, Higuchi M, Suhara T, Tanioka Y (2008) Neurobehavioral protection by single dose l-deprenyl against MPTP-induced parkinsonism in common marmosets. Psychopharmacology 195:509-516.
2. Arnold SE, Han LY, Clark CM, Grossman M, Trojanowski JQ (2000) Quantitative neurohistological features of frontotemporal degeneration. Neurobiol Aging 21:913-919.
3. Ban EM, Sarliève LL, Haour FG (1993) Interleukin-1 binding sites on astrocytes. Neuroscience 52:725-733.
4. Banati RB (2002) Visualising microglial activation in vivo. Glia 40:206-217.
5. Banati RB, Newcombe J, Gunn RN, Cagnin A, Turkheimer F, Heppner F, Price G, Wegner F, Giovannoni G, Miller DH, Perkin GD, Smith T, Hewson AK, Bydder G, Kreutzberg GW, Jones T, Cuzner ML, Myers R (2000) The peripheral benzodiazepine binding site in the brain in multiple sclerosis: quantitative in vivo imaging of microglia as a measure of disease activity. Brain 123:2321-2337.
6. Batchelor PE, Liberatore GT, Wong JY, Porritt MJ, Frerichs F, Donnan GA, Howells DW (1999) Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor. J Neurosci 19:1708-1716.
7. Cagnin A, Brooks DJ, Kennedy AM, Gunn RN, Myers R, Turkheimer FE, Jones T, Banati RB (2001) In-vivo measurement of activated microglia in dementia. Lancet 358:461-467.
8. Chen MK, Baidoo K, Verina T, Guilarte TR (2004) Peripheral benzodiazepine receptor imaging in CNS demyelination: functional implications of anatomical and cellular localization. Brain 127:1379-1392.
9. Combs CK, Johnson DE, Karlo JC, Cannady SB, Landreth GE (2000) Inflammatory mechanisms in Alzheimer's disease: inhibition of beta-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARgamma agonists. J Neurosci 20:558-567.
10. Constam DB, Philipp J, Malipiero UV, ten Dijke P, Schachner M, Fontana A (1992) Differential expression of transforming growth factor-beta 1, -beta 2, and -beta 3 by glioblastoma cells, astrocytes, and microglia. J Immunol 148:1404-1410.
11. Depino AM, Earl C, Kaczmarczyk E, Ferrari C, Besedovsky H, del Rey A, Pitossi FJ, Oertel WH (2003) Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson's disease. Eur J Neurosci 18:2731-2742.
12. Dickson DW, Lee SC, Mattiace LA, Yen SH, Brosnan C (1993) Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia 7:75-83.
13. Dodel RC, Hampel H, Du Y (2003) Immunotherapy for Alzheimer's disease. Lancet Neurol 2:215-220.
14. Elkabes S, DiCicco-Bloom EM, Black IB (1996) Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16:2508-2521.
15. Ferzaz B, Brault E, Bourliaud G, Robert JP, Poughon G, Claustre Y, Marguet F, Liere P, Schumacher M, Nowicki JP, Fournier J, Marabout B, Sevrin M, George P, Soubrie P, Benavides J, Scatton B (2002) SSR180575 (7-chloro-N,N,5-trimethyl-4-oxo-3-phenyl-3,5-dihydro-4H-pyridazino-[4,5-b] indole-1-acetamide), a peripheral benzodiazepine receptor ligand, promotes neuronal survival and repair. J Pharmacol Exp Ther 301:1067-1078.
16. Fiala M, Cribbs DH, Rosenthal M, Bernard G (2007) Phagocytosis of amyloid-beta and inflammation: two faces of innate immunity in Alzheimer's disease. J Alzheimers Dis 11:457-463.
17. Fujimura Y, Ikoma Y, Yasuno F, Suhara T, Ota M, Matsumoto R, Nozaki S, Takano A, Kosaka J, Zhang MR, Nakao R, Suzuki K, Kato N, Ito H (2006) Quantitative analyses of 18F-FEDAA1106 binding to peripheral benzodiazepine receptors in living human brain. J Nucl Med 47:43-50.
18. Gash DM, Zhang Z, Ovadia A, Cass WA, Yi A, Simmerman L, Russell D, Martin D, Lapchak PA, Collins F, Hoffer BJ, Gerhardt GA (1996) Functional recovery in parkinsonian monkeys treated with GDNF. Nature 380:252-255.
19. Gill SS, Patel NK, Hotton GR, O'Sullivan K, McCarter R, Bunnage M, Brooks DJ, Svendsen CN, Heywood P (2003) Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat Med 9:589-595.
20. Halldin C, Erixon-Lindroth N, Pauli S, Chou YH, Okubo Y, Karlsson P, Lundkvist C, Olsson H, Guilloteau D, Emond P, Farde L (2003) [(11)C]PE2I: a highly selective radioligand for PET examination of the dopamine transporter in monkey and human brain. Eur J Nucl Med Mol Imaging 30:1220-1230.
21. Hurley SD, O'Banion MK, Song DD, Arana FS, Olschowka JA, Haber SN (2003) Microglial response is poorly correlated with neurodegeneration following chronic, low-dose MPTP administration in monkeys. Exp Neurol 184:659-668.
22. Ikoma Y, Yasuno F, Ito H, Suhara T, Ota M, Toyama H, Fujimura Y, Takano A, Maeda J, Zhang MR, Nakao R, Suzuki K (2007) Quantitative analysis for estimating binding potential of the peripheral benzodiazepine receptor with [(11)C]DAA1106. J Cereb Blood Flow Metab 27:173-184.
23. Imai F, Suzuki H, Oda J, Ninomiya T, Ono K, Sano H, Sawada M (2007) Neuroprotective effect of exogenous microglia in global brain ischemia. J Cereb Blood Flow Metab 27:488-500.
24. Inaji M, Okauchi T, Ando K, Maeda J, Nagai Y, Yoshizaki T, Okano H, Nariai T, Ohno K, Obayashi S, Higuchi M, Suhara T (2005) Correlation between quantitative imaging and behavior in unilaterally 6-OHDA-lesioned rats. Brain Res 1064:136-145.
25. Kim YS, Joh TH (2006) Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease. Exp Mol Med 38:333-347.
26. Kito S, Noguchi Y, Ohta Y (2003) Developmental responses of two substrains of in vitro fertilized C57BL/6J mouse embryos to oxygen and amino acids. Exp Anim 52:63-66.
27. Knott C, Stern G, Kingsbury A, Welcher AA, Wilkin GP (2002) Elevated glial brain-derived neurotrophic factor in Parkinson's diseased nigra. Parkinsonism Relat Disord 8:329-341.
28. Kordower JH, Emborg ME, Bloch J, Ma SY, Chu Y, Leventhal L, McBride J, Chen EY, Palfi S, Roitberg BZ, Brown WD, Holden JE, Pyzalski R, Taylor MD, Carvey P, Ling Z, Trono D, Hantraye P, Déglon N, Aebischer P (2000) Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson's disease. Science 290:767-773.
29. Maeda J, Higuchi M, Inaji M, Ji B, Haneda E, Okauchi T, Zhang MR, Suzuki K, Suhara T (2007a) Phase-dependent roles of reactive microglia and astrocytes in nervous system injury as delineated by imaging of peripheral benzodiazepine receptor. Brain Res 1157:100-111.
30. Maeda J, Ji B, Irie T, Tomiyama T, Maruyama M, Okauchi T, Staufenbiel M, Iwata N, Ono M, Saido TC, Suzuki K, Mori H, Higuchi M, Suhara T (2007b) Longitudinal, quantitative assessment of amyloid, neuroinflammation, and anti-amyloid treatment in a living mouse model of Alzheimer's disease enabled by positron emission tomography. J Neurosci 27:10957-10968.
31. Marx J (2007) Alzheimer's disease. A new take on tau. Science 316:1416-1417.
32. Masliah E, Mallory M, Hansen L, Alford M, Albright T, DeTeresa R, Terry R, Baudier J, Saitoh T (1991) Patterns of aberrant sprouting in Alzheimer's disease. Neuron 6:729-739.
33. Matsushima GK, Morell P (2001) The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol 11:107-116.
34. McGeer EG, McGeer PL (2003) Inflammatory processes in Alzheimer's disease. Prog Neuropsychopharmacol Biol Psychiatry 27:741-749.
35. McGeer PL, Itagaki S, Boyes BE, McGeer EG (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 38:1285-1291.
36. Mills CD, Bitler JL, Woolf CJ (2005) Role of the peripheral benzodiazepine receptor in sensory neuron regeneration. Mol Cell Neurosci 30:228-237.
37. Mirza B, Hadberg H, Thomsen P, Moos T (2000) The absence of reactive astrocytosis is indicative of a unique inflammatory process in Parkinson's disease. Neuroscience 95:425-432.
38. Mizuno T, Sawada M, Marunouchi T, Suzumura A (1994) Production of interleukin-10 by mouse glial cells in culture. Biochem Biophys Res Commun 205:1907-1915.
39. Mogi M, Togari A, Kondo T, Mizuno Y, Komure O, Kuno S, Ichinose H, Nagatsu T (1999) Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson's disease. Neurosci Lett 270:45-48.
40. Mogi M, Togari A, Kondo T, Mizuno Y, Kogure O, Kuno S, Ichinose H, Nagatsu T (2001) Glial cell line-derived neurotrophic factor in the substantia nigra from control and parkinsonian brains. Neurosci Lett 300:179-181.
41. Myers R, Manjil LG, Cullen BM, Price GW, Frackowiak RS, Cremer JE (1991) Macrophage and astrocyte populations in relation to [3H]PK 11195 binding in rat cerebral cortex following a local ischaemic lesion. J Cereb Blood Flow Metab 11:314-322.
42. Nakajima K, Tsuzaki N, Nagata K, Takemoto N, Kohsaka S (1992) Production and secretion of plasminogen in cultured rat brain microglia. FEBS Lett 308:179-182.
43. Nelson PT, Soma LA, Lavi E (2002) Microglia in diseases of the central nervous system. Ann Med 34:491-500.
44. O'Callaghan JP, Miller DB, Reinhard JF Jr (1990) Characterization of the origins of astrocyte response to injury using the dopaminergic neurotoxicant, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Brain Res 521:73-80.
45. Pappata S, Levasseur M, Gunn RN, Myers R, Crouzel C, Syrota A, Jones T, Kreutzberg GW, Banati RB (2000) Thalamic microglial activation in ischemic stroke detected in vivo by PET and [11C]PK1195. Neurology 55:1052-1054.
46. Phinney AL, Deller T, Stalder M, Calhoun ME, Frotscher M, Sommer B, Staufenbiel M, Jucker M (1999) Cerebral amyloid induces aberrant axonal sprouting and ectopic terminal formation in amyloid precursor protein transgenic mice. J Neurosci 19:8552-8559.
47. Pickel VM, Beckley SC, Joh TH, Reis DJ (1981) Ultrastructural immunocytochemical localization of tyrosine hydroxylase in the neostriatum. Brain Res 225:373-385.
48. Qin L, Liu Y, Cooper C, Liu B, Wilson B, Hong JS (2002) Microglia enhance beta-amyloid peptide-induced toxicity in cortical and mesencephalic neurons by producing reactive oxygen species. J Neurochem 83:973-983.
49. Rojas S, Martín A, Arranz MJ, Pareto D, Purroy J, Verdaguer E, Llop J, Gómez V, Gispert JD, Millán O, Chamorro A, Planas AM (2007) Imaging brain inflammation with [(11)C]PK11195 by PET and induction of the peripheral-type benzodiazepine receptor after transient focal ischemia in rats. J Cereb Blood Flow Metab 27:1975-1986.
50. Sawada M, Imai F, Suzuki H, Hayakawa M, Kanno T, Nagatsu T (1998) Brain-specific gene expression by immortalized microglial cell-mediated gene transfer in the mammalian brain. FEBS Lett 433:37-40.
51. Sawada M, Imamura K, Nagatsu T (2006) Role of cytokines in inflammatory process in Parkinson's disease. J Neural Transm Suppl:373-381.
52. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Liao Z, Lieberburg I, Motter R, Mutter L, Soriano F, Shopp G, Vasquez N, Vandevert C, Walker S, Wogulis M, Yednock T, Games D, Seubert P (1999) Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400:173-177.
53. Smith ME (1999) Phagocytosis of myelin in demyelinative disease: a review. Neurochem Res 24:261-268.
54. Stephenson DT, Schober DA, Smalstig EB, Mincy RE, Gehlert DR, Clemens JA (1995) Peripheral benzodiazepine receptors are colocalized with activated microglia following transient global forebrain ischemia in the rat. J Neurosci 15:5263-5274.
55. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, Rothacher S, Ledermann B, Bürki K, Frey P, Paganetti PA, Waridel C, Calhoun ME, Jucker M, Probst A, Staufenbiel M, Sommer B (1997) Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci U S A 94:13287-13292.
56. Suzuki H, Imai F, Kanno T, Sawada M (2001) Preservation of neurotrophin expression in microglia that migrate into the gerbil's brain across the blood-brain barrier. Neurosci Lett 312:95-98.
57. Suzumura A, Sawada M, Yamamoto H, Marunouchi T (1993) Transforming growth factor-beta suppresses activation and proliferation of microglia in vitro. J Immunol 151:2150-2158.
58. Teismann P, Tieu K, Cohen O, Choi DK, Wu DC, Marks D, Vila M, Jackson-Lewis V, Przedborski S (2003) Pathogenic role of glial cells in Parkinson's disease. Mov Disord 18:121-129.
59. Tomac A, Lindqvist E, Lin LF, Ogren SO, Young D, Hoffer BJ, Olson L (1995) Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 373:335-339.
60. Van Dam D, Vloeberghs E, Abramowski D, Staufenbiel M, De Deyn PP (2005) APP23 mice as a model of Alzheimer's disease: an example of a transgenic approach to modeling a CNS disorder. CNS Spectr 10:207-222.
61. Venneti S, Lopresti BJ, Wang G, Slagel SL, Mason NS, Mathis CA, Fischer ML, Larsen NJ, Mortimer AD, Hastings TG, Smith AD, Zigmond MJ, Suhara T, Higuchi M, Wiley CA (2007) 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 102:2118-2131.
62. Vilhardt F, Plastre O, Sawada M, Suzuki K, Wiznerowicz M, Kiyokawa E, Trono D, Krause KH (2002) The HIV-1 Nef protein and phagocyte NADPH oxidase activation. J Biol Chem 277:42136-42143.
63. Wilms H, Claasen J, Röhl C, Sievers J, Deuschl G, Lucius R (2003) Involvement of benzodiazepine receptors in neuroinflammatory and neurodegenerative diseases: evidence from activated microglial cells in vitro. Neurobiol Dis 14:417-424.
64. Wojtera M, Sikorska B, Sobow T, Liberski PP (2005) Microglial cells in neurodegenerative disorders. Folia Neuropathol 43:311-321.
65. Yoshiyama Y, Higuchi M, Zhang B, Huang SM, Iwata N, Saido TC, Maeda J, Suhara T, Trojanowski JQ, Lee VM (2007) Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 53:337-351.
66. Zhang MR, Kida T, Noguchi J, Furutsuka K, Maeda J, Suhara T, Suzuki K (2003) [(11)C]DAA1106: radiosynthesis and in vivo binding to peripheral benzodiazepine receptors in mouse brain. Nucl Med Biol 30:513-519.
67. 18F]fluoroethyl-5- methoxybenzyl)acetamide, for PET imaging of peripheral benzodiazepine receptor in primate brain. J Med Chem 47:2228-2235.
68. Zilka N, Ferencik M, Hulin I (2006) Neuroinflammation in Alzheimer's disease: protector or promoter? Bratisl Lek Listy 107:374-383.
69. Ziv Y, Avidan H, Pluchino S, Martino G, Schwartz M (2006) Synergy between immune cells and adult neural stem/progenitor cells promotes functional recovery from spinal cord injury. Proc Natl Acad Sci U S A 103:13174-13179.