Complex motor disturbances in a sequential double lesion rat model of striatonigral degeneration (multiple system atrophy)

Neuroscience

Volumn 99, Issue 1, 2000, Pages 43-54

  Scherfler, C ^a   Puschban, Z ^a   Ghorayeb, I ^c   Goebel, G P ^d   Tison, F ^c   Jellinger, K ^b   Poewe, W ^a   Wenning, G K ^a  

^a UNIVERSITY HOSPITAL INNSBRUCK   (Austria)

^b LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

^c CNRS   (France)

^d Inst of Biostatist and Docum   (Austria)

Author keywords

6 hydroxydopamine; Balance test; Neuroprotection; Quinolinic acid; Staircase test; Stepping test

Indexed keywords

OXIDOPAMINE; QUINOLINIC ACID;

AKINESIA; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY EQUILIBRIUM; BRAIN INJURY; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; HISTOLOGY; LOCOMOTION; MALE; NERVE DEGENERATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; RAT; SHY DRAGER SYNDROME;

ANIMALS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; MOTOR ACTIVITY; MULTIPLE SYSTEM ATROPHY; OXIDOPAMINE; QUINOLINIC ACID; RATS; RATS, WISTAR; STRIATONIGRAL DEGENERATION; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE;

EID: 0034718190     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(00)00171-8     Document Type: Article

References (75)

1. Antonini A., Leenders K.L., Vontobel P., Maguire R.P., Missimer J., Psylla M., Gunther I. Complementary PET studies of striatal neuronal function in the differential diagnosis between multiple system atrophy and Parkinson's disease. Brain. 120:1997;2187-2195.
2. Barker R., Dunnett S.B. Ibotenic acid lesions of the striatum reduce drug-induced rotation in the 6-hydroxydopamine-lesioned rat. Expl Brain Res. 101:1994;365-374.
3. Barneoud P., Parmentier S., Mazadier M., Miquet J.M., Boireau A., Dubedat P., Blanchard J.C. Effects of complete and partial lesions of the dopaminergic mesotelencephalic system on skilled forelimb use in the rat. Neuroscience. 67:1995;837-848.
4. Ben-Shlomo Y., Wenning G.K., Tison F., Quinn N.P. Survival of patients with pathologically proven multiple system atrophy: a meta-analysis. Neurology. 48:1997;384-393.
5. Buisson A., Callebert J., Mathieu E., Plotkine M., Boulu R.G. Striatal protection induced by lesioning the substantia nigra of rats subjected to focal ischemia. J. Neurochem. 59:1992;1153-1157.
6. Buisson A., Pateau V., Plotkine M., Boulu R.G. Nigrostriatal pathway modulates striatum vulnerability to quinolinic acid. Neurosci. Lett. 131:1991;257-259.
7. Cairns N.J., Atkinson P.F., Hanger D.P., Anderton B.H., Daniel S.E., Lantos P.L. Tau protein in the glial cytoplasmic inclusions of multiple system atrophy can be distinguished from abnormal tau in Alzheimer's disease. Neurosci. Lett. 230:1997;49-52.
8. Castellani R. Multiple system atrophy: clues from inclusions. Am. J. Path. 153:1998;671-676.
9. Chang J.W., Wachtel S.R., Young D., Kang U.J. Biochemical and anatomical characterization of forepaw adjusting steps in rat models of Parkinson's disease: studies on medial forebrain bundle and striatal lesions. Neuroscience. 88:1999;617-628.
10. Clemens J.A., Phebus L.A. Dopamine depletion protects striatal neurons from ischemia-induced cell death. Life Sci. 42:1988;707-713.
11. Daniel S. E. (1992) Multiple system atrophy. In Autonomic Failure - A Textbook of Clinical Disorders of Autonomic Nervous System (eds Bannister R. and Mathias C.). Oxford Medical, Oxford.
12. Dunnett S.B., Isacson O., Sirinathsinghji D.J., Clarke D.J., Bjorklund A. Striatal grafts in rats with unilateral neostriatal lesions - III. Recovery from dopamine-dependent motor asymmetry and deficits in skilled paw reaching. Neuroscience. 24:1988;813-820.
13. Dunnett S.B., Iversen S.D. Sensorimotor impairments following localized kainic acid and 6-hydroxydopamine lesions of the neostriatum. Brain Res. 248:1982;121-127.
14. Fearnley J.M., Lees A.J. Striatonigral degeneration. A clinicopathological study. Brain. 113:1990;1823-1842.
15. Fisher R.S., Shiota C., Levine M.S., Hull C.D., Buchwald N.A. Interhemispheric organization of corticocaudate projections in the cat: a retrograde double-labelling study. Neurosci. Lett. 48:1984;369-373.
16. Fricker R.A., Annett L.E., Torres E.M., Dunnett S.B. The placement of a striatal ibotenic acid lesion affects skilled forelimb use and the direction of drug-induced rotation. Brain Res. Bull. 41:1996;409-416.
17. Friehs G.M., Parker R.G., He L.S., Haines S.J., Turner D.A., Ebner T.J. Lesioning of the striatum reverses motor asymmetry in the 6-hydroxydopamine rodent model of Parkinsonism. J. Neural Transplant. Plast. 2:1991;141-156.
18. Geneser-Jensen F.A., Blackstad T.W. Distribution of acetyl cholinesterase in the hippocampal region of the guinea pig. I. Entorhinal area, parasubiculum, and presubiculum. Z. Zellforsch. mikrosk. Anat. 114:1971;460-481.
19. Gerfen C.R., Staines W.A., Arbuthnott G.W., Fibiger H.C. Crossed connections of the substantia nigra in the rat. J. comp. Neurol. 207:1982;283-303.
20. Globus M.Y., Busto R., Dietrich W.D., Martinez E., Valdes I., Ginsberg M.D. Effect of ischemia on the in vivo release of striatal dopamine, glutamate, and gamma-aminobutyric acid studied by intracerebral microdialysis. J. Neurochem. 51:1988;1455-1464.
21. Globus M.Y., Ginsberg M.D., Dietrich W.D., Busto R., Scheinberg P. Substantia nigra lesion protects against ischemic damage in the striatum. Neurosci. Lett. 80:1987;251-256.
22. Goto S., Hirano A., Rojas Corona R.R. Immunohistochemical visualization of afferent nerve terminals in human globus pallidus and its alteration in neostriatal neurodegenerative disorders. Acta neuropath. Berl. 78:1989;543-550.
23. Goto S., Matsumoto S., Ushio Y., Hirano A. Subregional loss of putaminal efferents to the basal ganglia output nuclei may cause Parkinsonism in striatonigral degeneration. Neurology. 47:1996;1032-1036.
24. Holms S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6:1979;65-70.
25. Hughes A.J., Colosimo C., Kleedorfer B., Daniel S.E., Lees A.J. The dopaminergic response in multiple system atrophy. J. Neurol. Neurosurg. Psychiat. 55:1992;1009-1013.
26. Ilinsky I.A., Kultas-Ilinsky K., Rosina A., Haddy M. Quantitative evaluation of crossed and uncrossed projections from basal ganglia and cerebellum to the cat thalamus. Neuroscience. 21:1987;207-227.
27. Ito H., Kusaka H., Matsumoto S., Imai T. Striatal efferent involvement and its correlation to levodopa efficacy in patients with multiple system atrophy. Neurology. 47:1996;1291-1299.
28. Kerkerian L., Dusticier N., Nieoullon A. Modulatory effect of dopamine on high-affinity glutamate uptake in the rat striatum. J. Neurochem. 48:1987;1301-1306.
29. Kirik D., Rosenblad C., Bjorklund A. Characterization of behavioural and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Expl Neurol. 152:1998;259-277.
30. Kume A., Takahashi A., Hashizume Y. Neuronal cell loss of the striatonigral system in multiple system atrophy. J. Neurol. Sci. 117:1993;33-40.
31. Künzle H. Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. Brain Res. 88:1975;195-209.
32. Lang A.E., Curran T., Provias J., Bergeron C. Striatonigral degeneration: iron deposition in putamen correlates with the slit-like void signal of magnetic resonance imaging [published erratum appears in Can. J. neurol. Sci. (1995) 22, 73-74]. Can. J. neurol. Sci. 21:1994;311-318.
33. Lantos P.L., Papp M.I. Cellular pathology of multiple system atrophy: a review. J. Neurol. Neurosurg. Psychiat. 57:1994;129-133.
34. Lee C.S., Sauer H., Bjorklund A. Dopaminergic neuronal degeneration and motor impairments following axon terminal lesion by instrastriatal 6-hydroxydopamine in the rat. Neuroscience. 72:1996;641-653.
35. Leigh P.N., Reavill C., Jenner P., Marsden C.D. Basal ganglia outflow pathways and circling behaviour in the rat. J. neural Transm. 58:1983;1-41.
36. Lindner M.D., Plone M.A., Francis J.M., Emerich D.F. Validation of a rodent model of Parkinson's disease: evidence of a therapeutic window for oral Sinemet. Brain Res. Bull. 39:1996;367-372.
37. Marshall J.F., Ungerstedt U. Striatal efferent fibers play a role in maintaining rotational behaviour in the rat. Science. 198:1977;62-64.
38. Montoya C.P., Astell S., Dunnett S.B. Effects of nigral and striatal grafts on skilled forelimb use in the rat. Prog. Brain Res. 82:1990;459-466.
39. Montoya C.P., Campbell Hope L.J., Pemberton K.D., Dunnett S.B. The "staircase test": a measure of independent forelimb reaching and grasping abilities in rats. J. Neurosci. Meth. 36:1991;219-228.
40. Nakamura S., Kawamoto Y., Nakano S., Akiguchi I., Kimura J. Cyclin-dependent kinase 5 and mitogen-activated protein kinase in glial cytoplasmic inclusions in multiple system atrophy. J. Neuropath. exp. Neurol. 57:1998;690-698.
41. Nakao N., Brundin P. Effects of alpha-phenyl-tert-butyl nitrone on neuronal survival and motor function following intrastriatal injections of quinolinate or 3-nitropropionic acid. Neuroscience. 76:1997;749-761.
42. Nikkhah G., Duan W.M., Knappe U., Jodicke A., Bjorklund A. Restoration of complex sensorimotor behaviour and skilled forelimb use by a modified nigral cell suspension transplantation approach in the rat Parkinson model. Neuroscience. 56:1993;33-43.
43. Nitsch C., Wolfrum G., Schaefer F., Scotti A.L., Unger J. Opposite effects of intranigral ibotenic acid and 6-hydroxydopamine on motor behavior and on striatal neuropeptide Y neurons. Brain Res. Bull. 30:1993;21-32.
44. Olsson M., Nikkhah G., Bentlage C., Bjorklund A. Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J. Neurosci. 15:1995;3863-3875.
45. Parenti M., Rusconi L., Cappabianca V., Parati E.A., Groppetti A. Role of dopamine in manganese neurotoxicity. Brain Res. 473:1988;236-240.
46. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 2nd edn :1986;Academic, San Diego.
47. Pisa M. Motor functions of the striatum in the rat: critical role of the lateral region in tongue and forelimb reaching. Neuroscience. 24:1988;453-463.
48. Pisa M., Schranz J.A. Dissociable motor roles of the rat's striatum conform to a somatotopic model. Behav. Neurosci. 102:1988;429-440.
49. Price A.W., Fowler S.C. Deficits in contralateral and ipsilateral forepaw motor control following unilateral motor cortical ablations in rats. Brain Res. 205:1981;81-90.
50. Probst Cousin S., Rickert C.H., Schmid K.W., Gullotta F. Cell death mechanisms in multiple system atrophy. J. Neuropath. expl Neurol. 57:1998;814-821.
51. Puschban Z., Scherfler C., Granata R., Laboyrie P., Quinn N.P., Jenner P., Poewe W., Wenning G.K. Autoradiographic study of striatal dopamine reuptake sites and dopamine D1 and D2 receptors in a 6-hydroxydopamine and quinolinic acid double-lesion rat model of striatonigral degeneration (multiple system atrophy) and effects of embryonic ventral mesencephalic, striatal or co-grafts. Neuroscience. 95:2000;377-388.
52. Quinn N.P., Marsden C.D. The motor disorder of multiple system atrophy [published erratum appears in J. Neurol. Neurosurg. Psychiat. (1994) 57, 666]. J. Neurol. Neurosurg. Psychiat. 56:1993;1239-1242.
53. Rosenberg P.A. Catecholamine toxicity in cerebral cortex in dissociated cell culture. J. Neurosci. 8:1988;2887-2894.
54. Schallert T., Norton D., Jones T.A. A clinically relevant unilateral rat model of Parkinsonian akinesia. J. neural Transpl. Plast. 3:1992;332-333.
55. Schallert T., Hall S. Disengage sensorimotor deficit following apparent recovery from unilateral dopamine depletion. Behav. Brain Res. 30:1988;15-24.
56. Schmidt R.H., Bjorklund A., Stenevi U., Dunnett S.B., Gage F.H. Intracerebral grafting of neuronal cell suspensions. III. Activity of intrastriatal nigral suspension implants as assessed by measurements of dopamine synthesis and metabolism. Acta physiol. Scand. Suppl. 522:1983;19-28.
57. Schwarcz R., Fuxe K., Agnati L.F., Hokfelt T., Coyle J.T. Rotational behaviour in rats with unilateral striatal kainic acid lesions: a behavioural model for studies on intact dopamine receptors. Brain Res. 170:1979;485-495.
58. Schwarting R.K., Huston J.P. The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments. Prog. Neurobiol. 50:1996;275-331.
59. Schwarz S.C., Seufferlein T., Liptay S., Schmid R.M., Kasischke K., Foster O.J.F., Daniel S.E., Schwarz J. Microglial activation in multiple system atrophy: a potential role for NF-kB/rel proteins. NeuroReport. 9:1998;3023-3029.
60. Slivka A., Cohen G. Hydroxyl radical attack on dopamine. J. biol. Chem. 260:1985;15,466-15,472.
61. Spillantini M.G., Tolnay M., Love S., Goedert M. Microtubule-associated protein tau, heparan sulphate and alpha-synuclein in several neurodegenerative diseases with dementia. Acta neuropath., Berlin. 97:1999;585-594.
62. Tison F., Wenning G.W., Daniel S.E., Quinn N.P. The pathophysiology of Parkinsonism in multiple system atrophy. Eur. J. Neurol. 2:1995;435-444.
63. Tossman U., Segovia J., Ungerstedt U. Extracellular levels of amino acids in striatum and globus pallidus of 6-hydroxydopamine-lesioned rats measured with microdialysis. Acta physiol. scand. 127:1986;547-551.
64. Tu P.H., Galvin J.E., Baba M., Giasson B., Tomita T., Leight S., Nakajo S., Iwatsubo T., Trojanowski J.Q., Lee V.M. Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble alpha-synuclein. Ann. Neurol. 44:1998;415-422.
65. van der Eecken H., Adams R.D., van Bogaert L. Striopallidal-nigral degeneration. An hitherto undescribed lesion in paralysis agitans. J. neural Transpl. Plast. 19:1960;159-161.
66. Venero J.L., Romero Ramos M., Revuelta M., Machado A., Cano J. Intrastriatal quinolinic acid injections protect against 6-hydroxydopamine-induced lesions of the dopaminergic nigrostriatal system. Brain Res. 672:1995;153-158.
67. Wenning G.K., Tison F., Scherfler C., Puschban Z., Waldner R., Granata R., Gorayeb I., Poewe W. Towards neurotransplantation in multiple system atrophy: clinical rational, pathophysiological basis and preliminary experimental evidence. Cell Transplant. 9:2000;279-288.
68. Wenning G.K., Ben Shlomo Y., Magalhaes M., Daniel S.E., Quinn N.P. Clinical features and natural history of multiple system atrophy. An analysis of 100 cases. Brain. 117:1994;835-845.
69. Wenning G.K., Granata R., Laboyrie P.M., Quinn N.P., Jenner P., Marsden C.D. Reversal of behavioural abnormalities by fetal allografts in a novel rat model of striatonigral degeneration. Mov. Disord. 11:1996;522-532.
70. Wenning G.K., Granata R., Puschban Z., Scherfler C., Poewe W. Neural transplantation in animal models of multiple system atrophy: a review. J. neural Transm. Suppl. 55:1999;103-113.
71. Wenning G.K., Tison F., Ben Shlomo Y., Daniel S.E., Quinn N.P. Multiple system atrophy: a review of 203 pathologically proven cases. Mov. Disord. 12:1997;133-147.
72. Whishaw I.Q., O'Connor W.T., Dunnett S.B. The contributions of motor cortex, nigrostriatal dopamine and caudate-putamen to skilled forelimb use in the rat. Brain. 109:1986;805-843.
73. Winkler C., Bentlage C., Nikkhah G., Samii M., Bjorklund A. Intranigral transplants of GABA-rich striatal tissue induce behavioral recovery in the rat Parkinson model and promote the effects obtained by intrastriatal dopaminergic transplants. Expl Neurol. 155:1999;165-186.
74. Winkler C., Sauer H., Lee C.S., Bjorklund A. Short-term GDNF treatment provides long-term rescue of lesioned nigral dopaminergic neurons in a rat model of Parkinson's disease. J. Neurosci. 16:1996;7206-7215.
75. Wullner U., Young A.B., Penney J.B., Beal M.F. 3-Nitropropionic acid toxicity in the striatum. J. Neurochem. 63:1994;1772-1781.