Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging

European Journal of Neuroscience

Volumn 15, Issue 6, 2002, Pages 991-998

  Cicchetti, F ^a   Brownell, A L ^a,b   Williams, K ^a   Chen, Y I ^b   Livni, E ^b   Isacson, Ole ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

6 OHDA; Inflammation; Parkinson's disease; PET imaging; PK11195; Sprague Dawley rats

Indexed keywords

3BETA (4 FLUOROPHENYL) 2BETA TROPANECARBOXYLIC ACID METHYL ESTER; ANTIBODY; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; OXIDOPAMINE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BRAIN NERVE CELL; CADAVER; CELL ACTIVATION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; ENCEPHALITIS; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MICROGLIA; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RAT; SUBSTANTIA NIGRA;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD147; ANTIGENS, NEOPLASM; ANTIGENS, SURFACE; ANTINEOPLASTIC AGENTS; AVIAN PROTEINS; BLOOD PROTEINS; CARBON RADIOISOTOPES; DOPAMINE; ENCEPHALITIS; GLIOSIS; ISOQUINOLINES; MEMBRANE GLYCOPROTEINS; MICROGLIA; NEOSTRIATUM; NEURAL PATHWAYS; NEURONS; OXIDOPAMINE; PARKINSON DISEASE; RATS; SUBSTANTIA NIGRA; SYMPATHOLYTICS; TOMOGRAPHY, EMISSION-COMPUTED; TYROSINE 3-MONOOXYGENASE;

EID: 0036459335     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.01938.x     Document Type: Article

References (41)

1. Abercrombie, M. (1946) Estimation of nuclear populations from microtome sections. Anat. Rec., 94, 239-247.
2. Akiyama, H. & McGeer, P.L. (1989) Microglial response to 6-hydroxydopamine-induced substantia nigra lesions. Brain Res., 489, 247-253.
3. Banati, R.B., Daniel, S.E. & Blunt, S.B. (1998) Glial pathology but absence of apoptotic nigral neurons in long-standing Parkinson's disease. Mov. Disord., 13, 221-227.
4. Banati, R.B., Goerres, G.W., Myers, R., Gunn, R.N., Turkheimer, F.E., Kreutzberg, G.W., Brooks, D.J., Jones, T. & Duncan, J.S. (1999) [11C] (R) - PK11195 positron emission tomography imaging of activated microglia in vivo in Rasmussen's encephalitis. Neurology, 53, 2199-2203.
5. Banati, R.B., Myers, R. & Kreutzberg, G.W. (1997) PK ('peripheral benzodiazepine') -binding sites in the CNS indicate early and discrete brain lesions: Microautoradiographic detection of [3H]PK11195 binding to activated microglia. J. Neurocytol., 26, 77-82.
6. Bjorklund, A., Rosenblad, C., Winkler, C. & Kirik, D. (1997) Studies on neuroprotective and regenerative effects of GDNF in a partial lesion model of Parkinson's disease. Neurobiol. Dis., 4, 186-200.
7. Bjorklund, L. & Stromberg, I. (1997) Dopaminergic innervation of striatal grafts placed into different sites of normal striatum: Differences in the tyrosine hydroxylase immunoreactive growth pattern. Exp. Brain Res., 113, 13-23.
8. Brooks, D., Banati, R.B., Cagnin, A., Myers, R., Gunn, R.N., Piccini, P., Olanow, C.W., Jones, T., & Brooks, D.J. (1999) In vivo detection of activated microglia by [11C]PD11195-PET indicates involvement of the globus pallidum in idiopathic Parkinson's disease. In Calne, D.B., (ed.), Parkinsonism and Related Disorders. Abstracts of the XIII International Congress on Parkinson's Disease, Vancouver, B.C., Elsevier Science Ltd, New York, pp. S56-57.
9. Brownell, G.L., Burnham, C.A. & Chesler, D.A. (1985) High resolution tomograph using analog coding. In Greitz, T., Ingvar, D.H., Widen, L. (eds), The Metabolism of the Human Brain Studied with Positron Emission Tomography. Raven Press, New York, NY, pp. 13-19.
10. Brownell, A.-L., Jenkins, B.G., Elmaleh, D.R., Deacon, T.W., Spealman, R.D. & Isacson, O. (1998a) Combined PET/MRS studies of the brain reveal dynamic and long-term physiological changes in a Parkinson's disease primate model. Nature Med., 4, 1308-1312.
11. Brownell, A.-L., Jenkins, B.G. & Isacson, O. (1999) Dopamine imaging markers and predictive mathematical models for progressive degeneration in Parkinson's disease. Biomed. Pharmacother., 53, 131-140.
12. Brownell, A.-L., Livni, E., Galpern, W.R. & Isacson, O. (1998b) In vivo PET imaging in rat of dopamine terminals reveals functional neural transplants. Ann. Neurol., 43, 387-390.
13. Cagnin, A., Brooks, D., Kennedy, A.M., Gunn, R.N., Myers, R., Turkheimer, F.E., Jones, T. & Banati, R.B. (2001) In-vivo measurement of activated microglia in dementia. The Lancet, 358, 461-467.
14. Camsonne, R., Crouzel, C., Comar, D., Maziere, M., Prenant, C., Sastre, J., Moulin, M.A. & Syrota, A. (1984) Synthesis of N-(11-C) methyl, N-(methyl-1 propyl), (chloro-2 phenyl) -1 isoquinoleine carboxamide-3 (PK11195): A new ligand for peripheral benzodiazepine receptors. J. Labelled Compounds Radiopharmaceuticals, XXI, 985-991.
15. Cappelli, A., Anzini, M., Vomero, S., De Benedetti, P.G., Menziani, M.C., Giorgi, G. & Manzoni, C. (1997) Mapping the peripheral benzodiazepine receptor binding site by conformationally restrained derivatives of 1-(2-chlorophenyl) -N-methyl-N-(1-methylpropyl) -3-isoquinolinecarboxamide (PK11195). J. Med. Chem., 40, 2910-2921.
16. Chen, S., Le, W.D., Xie, W.J., Alexianu, M.E., Engelhardt, J.I., Siklos, L. & Appel, S.H. (1998) Experimental destruction of substantia nigra initiated by Parkinson disease immunoglobulins. Arch. Neurol., 55, 1075-1080.
17. Costantini, L.C., Cole, D., Chaturvedi, P. & Isacson, O. (2001) Immunophilin ligands can prevent progressive dopaminergic degeneration in animal models of Parkinson's disease. Eur. J. Neurosci., 13, 1085-1092.
18. Czlonkowska, A., Kurkowska-Jastrzebska, I. & Czlonkowski, A. (1999) Inflammatory changes in the substantia nigra and striatum following MPTP intoxication. Ann. Neurol., 46, 598-605.
19. Gerhard, A., Banati, R.B., Cagnin, A. & Brooks, D.J. (2001) In vivo imaging of activated microglia with [11C]PK11195 positron emission tomography (PET) in idiopathic and atypical Parkinson's disease. Neurology, 56, A270.
20. Gerhard, A., Neumaier, B., Elitok, E., Glatting, G., Ries, V., Tomczak, R., Ludolph, A.C. & Reske, S.V. (2000) In vivo imaging of activated microglia using 11C-PK11195 and positron emission tomography in patients after ischemic stoke. Neuroreport, 11, 2957-2960.
21. Graeber, M.B., Bise, K. & Mehraein, P. (1993) Synaptic stripping in the human facial nucleus. Acta Neuropathol. (Berl.), 86, 179-181.
22. Graeber, M.B., Streit, W.J., Kiefer, R., Schoen, S.W. & Kreutzberg, G.W. (1990) New expression of myelomonocytic antigens by microglia and perivascular cells following lethal motor neuron injury. J. Neuroimmunol., 27, 121-132.
23. Hantraye, P., Brownell, A.-L., Elmaleh, D., Spealman, R.D., Wullner, U., Brownell, G.L. & Isacson, O. (1992) Dopamine fiber detection by [11C]-CFT and PET in a primate model of parkinsonism. Neuroreport, 3, 265-268.
24. Hirsch, E.C., Hunot, S., Damier, P. & Faucheux, B. (1998) Glial cells and inflammation in Parkinson's disease: A role in neurodegeneration? Ann. Neurol., 44, S115-S120.
25. Isacson, O., Fischer, W., Wictorin, K., Dawbarn, D., & Bjorklund, A. (1987) Astroglial response in the excitotoxically lesioned neostriatum and its projection areas in the rat. Neuroscience, 20, 1043-1056.
26. Junck, L., Olson, J.M.M., Ciliax, B.J., Koeppe, R.A., Warkins, G.L., Jewett, D.M., McKeever, P.E., Wieland, D.M., Kilbourn, M.R., Starosta-Rubinstein, S., Mancini, W.R., Kuhl, D.E., Greenberg, H.S. & Young, A.B. (1989) PET imaging of human gliomas with ligands for the peripheral benzodiazepine binding site. Ann. Neurol., 26, 752-758.
27. Kurkowska-Jastrzebska, I., Wronska, A., Kohutnicka, M., Czlonkowski, A. & Czlonkowska, A. (1999) The inflammatory reaction following 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine intoxication in mouse. Exp. Neurol., 156, 50-61.
28. Langston, J.W., Forno, L.S., Tetrud, J., Reeves, A.G., Kaplan, J.A. & Karluk, D. (1999) Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Ann. Neurol., 46, 598-605.
29. Lee, C.S., Sauer, H. & Bjorklund, A. (1996) Dopaminergic neuronal degeneration and motor impairments following axon terminal lesion by intrastriatal 6-hyroxydopamine in the rat. Neuroscience, 72, 641-653.
30. Lu, X., Bing, G. & Hagg, T. (2000) Naloxone prevents microglia-induced degeneration of dopaminergic substantia nigra neurons in the adult rats. Neuroscience, 97, 285-291.
31. Lue, L.F., Brachova, L., Civin, H. & Rogers, J. (1996) Inflammation, AB deposition, and neurofribrillary tangle formation as correlates of Alzheimer's disease neurodegeneration. J. Neuropathol. Exp. Neurol., 55, 1083-1088.
32. Mackenzie, I.R.A. (2000) Activated microglia in dementia with Lewy bodies. Neurology, 55, 132-134.
33. McGeer, P.L., Itagaki, S., Boyes, B.E. & McGeer, E.G. (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology, 38, 1285-1291.
34. McGeer, P.L., Itagaki, S., Tago, H. & McGeer, E.G. (1987) Reactive microglia in patients with senile dementia of the Alzheimer type are positive for the histocompatibility glycoprotein HLA-DR. Neurosci. Lett., 79, 195-200.
35. McGeer, E.G. & McGeer, P.L. (1998) The importance of inflammatory mechanisms in Alzheimer disease. Exp. Gerontol., 33, 371-378.
36. McGeer, P.L., Schwab, C., McGeer, E.G., Haddock, R.L. & Steele, J.C. (1997) Familial nature and continuing morbidity of the amyotrophic lateral sclerosis-parkinsonism dementia complex of Guam. Neurology, 49, 400-409.
37. McGeer, P.L., Yasojima, K. & McGeer, E.G. (2001) Inflammation in Parkinson's disease. Adv. Neurol., 86, 83-89.
38. Myers, R., Manjil, L.G., Frackowiak, R.S.J. & Cremer, J.E. (1991) [3H]PK11195 and the localisation of secondary thalamic lesions following focal ischaemia in rat motor cortex. Neurosci. Lett., 133, 20-24.
39. Pappata, S., Levasseur, M., Gunn, R.N., Myer, R., Crouzel, C., Syrota, A., Jones, T., Kreutzberg, G.W. & Banati, R.B. (2000) Thalamic microglial activation in ischemic stroke detected in vivo by PET and 11C-PK11195. Neurology, 55, 1052-1054.
40. Sauer, H. & Oertel, W.H. (1994) Progressive degeneration of nigrostriatal dopamine neurons following intrastriatal terminal lesions with 6-hydroxydopamine: A combined retrograde tracing and immunocytochemical study in the rat. Neuroscience, 59, 401-415.
41. Vowinckel, E., Reutens, D., Becher, B., Verge, G., Evans, A., Owens, T. & Antel, J.P. (1997) PK11195 binding to the peripheral benzodiazepine receptor as a marker of microglia activation in multiple sclerosis and experimental autoimmune encephalomyelitis. J. Neurosci. Res., 50, 345-353.