Timecourse of striatal re-innervation following lesions of dopaminergic SNpc neurons of the rat

European Journal of Neuroscience

Volumn 18, Issue 5, 2003, Pages 1175-1188

  Stanic, D ^a   Finkelstein, D I ^a,b   Bourke, D W ^a   Drago, J ^a,b   Horne, M K ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

6 OHDA; Dopamine; Plasticity; Sprouting; Timecourse

Indexed keywords

AMPHETAMINE; DOPAMINE; DOPAMINE TRANSPORTER; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL HEALTH; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CIRCLING BEHAVIOR; CONTROLLED STUDY; IMMUNOCOMPETENT CELL; MALE; MEDIAL FOREBRAIN BUNDLE; NERVE CELL LESION; NERVE ENDING; NERVE FIBER; NERVE SPROUTING; NERVOUS SYSTEM DEVELOPMENT; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REINNERVATION; SUBSTANTIA NIGRA;

ANIMALS; AXONS; BEHAVIOR, ANIMAL; BIOTIN; CELL COUNT; DEXTRANS; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; IMMUNOHISTOCHEMISTRY; MALE; MEDIAL FOREBRAIN BUNDLE; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURONS; OXIDOPAMINE; RATS; RATS, WISTAR; ROTATION; SUBSTANTIA NIGRA; SYMPATHOLYTICS; TIME FACTORS; TYROSINE 3-MONOOXYGENASE;

EID: 0038014518     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02800.x     Document Type: Article

References (61)

1. Agid, Y., Javoy, F. & Glowinski, J. (1973) Hyperactivity of remaining dopaminergic neurones after partial destruction of the nigro-striatal dopaminergic system in the rat. Nature, 245, 150-151.
2. Anglade, P., Mouatt-Prigent, A., Agid, Y. & Hirsch, E. (1996) Synaptic plasticity in the caudate nucleus of patients with Parkinson's disease. Neurodegeneration, 5, 121-128.
3. Betarbet, R., Sherer, T.B. & Greenamyre, J.T. (2002) Animal models of Parkinson's disease. Bioessays, 24, 308-318.
4. Bjorklund, A. & Lindvall, O. (1984) Dopamine-containing systems in the CNS. In Bjorklund, A. & Hokfelt, T. (Eds), Handbook of Chemical Neuroanatomy: Classical Transmitters in the CNS, Part 1. Elsevier, Amsterdam pp. 55-122.
5. Blanchard, V., Anglade, P., Dziewczapolski, G., Savasta, M., Agid, Y. & Raisman-Vozari, R. (1996) Dopaminergic sprouting in the rat striatum after partial lesion of the substantia nigra. Brain Res., 709, 319-325.
6. Blanchard, V., Chritin, M., Vyas, S., Savasta, M., Feuerstein, C., Agid, Y., Javoy-Agid, F. & Raisman-Vozari, R. (1995) Long-term induction of tyrosine hydroxylase expression: compensatory response to partial degeneration of the dopaminergic nigrostriatal system in the rat brain. J. Neurochem., 64, 1669-1679.
7. Bohn, M.C., Cupit, L., Marciano, F. & Gash, D.M. (1987) Adrenal medulla grafts enhance recovery of striatal dopaminergic fibers. Science, 237, 913-916.
8. Braendgaard, H., Evans, S.M., Howard, C.V. & Gundersen, H.J. (1990) The total number of neurons in the human neocortex unbiasedly estimated using optical disectors. J. Microsc., 157, 285-304.
9. Brecknell, J.E., Du Haque, N.S.J.S., Muir, E.M., Fidler, P.S., Hlavin, M.L., Fawcett, J.W. & Dunnett, S.B. (1996) Functional and anatomical reconstruction of the 6-hydroxydopamine lesioned nigrostriatal system of the adult rat. Neuroscience, 71, 913-925.
10. Cicchetti, F., Brownell, A.L., Williams, K., Chen, Y.I., Livni, E. & Isacson, O. (2002) Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging. Eur. J. Neurosci., 15, 991-998.
11. Ciliax, B.J., Drash, G.W., Staley, J.K., Haber, S., Mobley, C.J., Miller, G.W., Mufson, E.J., Mash, D.C. & Levey, A.I. (1999) Immunocytochemical localization of the dopamine transporter in human brain. J. Comp. Neurol., 409, 38-56.
12. Ciliax, B.J., Heilman, C., Demchyshyn, L.L., Pristupa, Z.B., Ince, E., Hersch, S.M., Niznik, H.B. & Levey, A.I. (1995) The dopamine transporter: immunochemical characterization and localization in brain. J. Neurosci., 15, 1714-1723.
13. Ciliax, B.J., Kilbourn, M.R., Haka, M.S. & Penney, J.B. Jr (1990) Imaging the dopamine uptake site with ex vivo [18F]GBR 13119 binding autoradiography in rat brain. J. Neurochem., 55, 619-623.
14. Coggeshall, R.E. & Lekan, H.A. (1996) Methods for determining numbers of cells and synapses: a case for more uniform standards of review [published erratum appears in J. Comp. Neurol. 1996 May 20; 369 (1): 162]. J. Comp. Neurol., 364, 6-15.
15. DeOlmos, J.S. & Ingram, N.R. (1971) An improved cupric-silver method for impregnation of axonal and terminal degeneration. Brain Res., 33, 523-529.
16. Deumens, R., Blokland, A. & Prickaerts, J. (2002) Modeling Parkinson's disease in rats: an evaluation of 6-OHDA lesions of the nigrostriatal pathway. Exp. Neurol., 175, 303-317.
17. Dravid, A., Jaton, A.L., Enz, A. & Frei, P. (1984) Spontaneous recovery from motor asymmetry in adult rats with 6-hydroxydopamine-induced partial lesions of the substantia nigra. Brain Res., 311, 361-365.
18. Fallon, J.H. & Moore, R.Y. (1978) Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. Comp. Neurol., 180, 545-580.
19. Finkelstein, D.I., Stanic, D., Parish, C.L., Tomas, D., Dickson, K. & Home, M.K. (2000) Axonal sprouting following lesions of the rat substantia nigra. Neuroscience, 97, 99-112.
20. Freed, C., Revay, R., Vaughan, R.A., Kriek, E., Grant, S., Uhl, G.R. & Kuhar, M.J. (1995) Dopamine transporter immunoreactivity in rat brain. J. Comp. Neurol., 359, 340-349.
21. Geffen, C.R., Baimbridge, K.G. & Thibault, J. (1987a) The neostriatal mosaic. III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems. J. Neurosci., 7, 3935-3944.
22. Geffen, C.R., Herkenham, M. & Thibault, J. (1987b) The neostriatal mosaic. II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J. Neurosci., 7, 3915-3934.
23. Gnanalingham, K.K., Milkowski, N.A., Smith, L.A., Hunter, A.J., Jenner, P. & Marsden, C.D. (1995) Short- and long-term changes in striatal and extra-striatal dopamine uptake sites in the MPTP-treated common marmoset. Eur. J. Pharmacol., 277, 235-241.
24. Hansen, J.T., Sakai, K., Greenamyre, J.T. & Moran, S. (1995) Sprouting of dopaminergic fibers from spared mesencephalic dopamine neurons in the unilateral partial lesioned rat. Brain Res., 670, 197-204.
25. Hastings, T., Lewis, D. & Zigmond, M. (1996) Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc. Natl Acad. Sci. USA, 93, 1956-1961.
26. Hefti, E, Melamed, E. & Wurtman, R.J. (1980) Partial lesions of the dopaminergic nigrostriatal system in rat brain: biochemical characterization. Brain Res., 195, 123-137.
27. Herges, S. & Taylor, D.A. (1999) Modulatory effect of p-chlorophenylalanine microinjected into the dorsal and median raphe nuclei on cocaine-induced behaviour in the rat. Eur. J. Pharmacol., 374, 329-340.
28. Hersch, S.M., Yi, H., Heilman, C.J., Edwards, R.H. & Levey, A.I. (1997) Subcellular localization and molecular topology of the dopamine transporter in the striatum and substantia nigra. J. Comp. Neurol., 388, 211-227.
29. Ichitani, Y., Okamura, H., Matsumoto, Y., Nagatsu, I. & Ibata, Y. (1991) Degeneration of the nigral dopamine neurons after 6-hydroxydopamine injection into the rat striatum. Brain Res., 549, 350-353.
30. Ingham, C.A., Hood, S.H., Taggart, P. & Arbuthnott, G.W. (1996) Synaptic plasticity in the rat neostriatum after unilateral 6-hydroxydopaminelesion of the nigrostriatal dopaminergic pathway. In Ohge, C., Kinura, M. & McKenzie, J.S. (Eds), The Basal Gangliav. Plenum Press, New York, 157-164.
31. Ingham, C.A., Hood, S.H., Taggart, P. & Arbuthnott, G.W. (1998) Plasticity of synapses in the rat neostriatum after unilateral lesion of the nigrostriatal dopaminergic pathway. J. Neurosci., 18, 4732-4743.
32. Kay, J.N. & Blum, M. (2000) Differential response of ventral midbrain and striatal progenitor cells to lesions of the nigrostriatal dopaminergic projection. Dev. Neurosci., 22, 56-67.
33. Kitt, C.A., Cork, L.C., Eidelberg, F., Joh, T.H. & Price, D.L. (1986) Injury of nigral neurons exposed to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine: a tyrosine hydroxylase immunocytochemical study in monkey. Neuroscience, 17, 1089-1103.
34. Lie, D.C., Dziewczapolski, G., Willhoite, A.R., Kaspar, B.K., Shults, C.W. & Gage, F.H. (2002) The adult substantia nigra contains progenitor cells with neurogenic potential. J. Neurosci., 22, 6639-6649.
35. Miller, G.W., Gainetdinov, R.R., Levey, A.I. & Caron, M.G. (1999) Dopamine transporters and neuronal injury. Trends Pharmacol. Sci., 20, 424-429.
36. Mitsumoto, Y., Watanabe, A., Mori, A. & Koga, N. (1998) Spontaneous regeneration of nigrostriatal dopaminergic neurons in MPTP-treated C57BL/6 mice. Biochem. Biophys. Res. Commun., 248, 660-663.
37. Nirenberg, M.J., Chan, J., Pohorille, A., Vaughan, R.A., Uhl, G.R., Kuhar, M.J. & Pickel, V.M. (1997a) The dopamine transporter: comparative ultrastructure of dopaminergic axons in limbic and motor compartments of the nucleus accumbens. J. Neurosci., 17, 6899-6907.
38. Nirenberg, M.J., Chan, J., Vaughan, R.A., Uhl, G.R., Kuhar, M.J. & Pickel, V.M. (1997b) Immunogold localization of the dopamine transporter: an ultrastructural study of the rat ventral tegmental area. J. Neurosci., 17, 5255-5262.
39. Parish, C.L., Finkelstein, D.I., Drago, J., Borrelli, E. & Horne, M.K. (2001) The role of dopamine receptors in regulating the size of axonal arbors. J. Neurosci., 21, 5147-5157.
40. Parish, C.L., Stanic, D., Drago, J., Borrelli, E., Finkelstein, D.I. & Horne, M.K. (2002) Effects of long-term treatment with dopamine receptor agonists and antagonists on terminal arbor size. Eur. J. Neurosci., 16, 787-794.
41. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Co-Ordinates, 3rd edn. Academic Press, Sydney.
42. Perese, D.A., Ulman, J., Viola, J., Ewing, S.E. & Bankiewicz, K.S. (1989) A 6-hydroxydopamine-induced selective parkinsonian rat model. Brain Res., 494, 285-293.
43. Pickel, V.M., Johnson, E., Carson, M. & Chan, J. (1992) Ultrastructure of spared dopamine terminals in caudate-putamen nuclei of adult rats neonatally treated with intranigral 6-hydroxydopamine. Brain Res. Dev. Brain Res., 70, 75-86.
44. Pycock, C.J. (1980) Turning behaviour in animals. Neuroscience, 5, 461-514.
45. Rabinovic, A., Lewis, D. & Hastings, T. (2000) Role of oxidative changes in the degeneration of dopamine terminals after injection of neurotoxic levels of dopamine. Neuroscience, 101, 67-76.
46. Sakai, K. & Gash, D.M. (1994) Effect of bilateral 6-OHDA lesions of the substantia nigra on locomotor activity in the rat. Brain Res., 633, 144-150.
47. Song, D.D. & Haber, S.N. (2000) Striatal responses to partial dopaminergic lesion: evidence for compensatory sprouting. J. Neurosci., 20, 5102-5114.
48. Stanic, D., Finkelstein, D.I., Parish, C.L., Zhu, W., Krstew, E., Drago, J., Lawrence, A.J. & Horne, M.K. (2002) Changes in function and ultrastructure of striatal dopaminergic terminals following partial lesions of the Snpc. [Abstract, FENS meeting, Paris 2002.] FENS, A186.116.
49. Stanic, D., Parish, C.L., Zhu, W., Krstew, E.V., Lawrence, A.J., Drago, J., Finkelstein, D.I. & Horne, M.K. (2003) Changes in function and ultrastructure of striatal dopaminergic terminals that regenerate following partial lesions of the Snpc. J. Neurochem., 86, 329-343.
50. Stanic, D., Tomas, D., Finkelstein, D.I. & Horne, M.K. (2000) Timecourse and initiation of sprouting in substantia nigra neurons. Soc. Neurosci. Abstract, 26, 794-798.
51. Thomas, J., Wang, J., Takubo, H., Sheng, J., de Jesus, S. & Bankiewicz, K.S. (1994) A 6-hydroxydopamine-induced selective parkinsonian rat model: further biochemical and behavioral characterization. Exp. Neurol., 126, 159-167.
52. Tripanichkul, W., Stanic, D., Drago, J., Finkelstein, D.I. & Horne, M.K. (2003) D2 Dopamine receptor blockade results in sprouting of DA axons in the intact animal but prevents sprouting following Nigral lesions. Eur. J. Neurosci., 17, 1-13.
53. Ungerstedt, U. (1968) 6-Hydroxy-dopamine induced degeneration of central monoamine neurons. Eur. J. Pharmacol., 5, 107-110.
54. Ungerstedt, U. & Arbuthnott, G.W. (1970) Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res., 24, 485-493.
55. Vizuete, M.L., Merino, M., Cano, J. & Machado, A. (1997) In vivo protection of striatal dopaminergic system against 1-methyl-4-phenylpyridinium neurotoxicity by phenobarbital. J. Neurosci. Res., 49, 301-308.
56. Wenning, G.K., Granata, R., Laboyrie, P.M., Quinn, N.P., Jenner, P. & Marsden, C.D. (1996) Reversal of behavioural abnormalities by fetal allografts in a novel rat model of striatonigral degeneration. Mov. Disord., 11, 522-532.
57. West, M.J. & Gundersen, H.J. (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol., 296, 1-22.
58. West, M.J., Slomianka, L. & Gundersen, H.J. (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec., 231, 482-497.
59. Wilson, J.M., Levey, A.I., Rajput, A., Ang, L., Guttman, M., Shannak, K., Niznik, H.B., Hornykiewicz, O., Pifl, C. & Kish, S.J. (1996) Differential changes in neurochemical markers of striatal dopamine nerve terminals in idiopathic Parkinson's disease. Neurology, 47, 718-726.
60. Yurek, D.M. (1997) Intranigral transplants of fetal ventral mesencephalic tissue attenuate D1-agonist-induced rotational behavior. Exp. Neurol., 143, 1-9.
61. Zhou, J., Pliego-Rivero, B., Bradford, H.F. & Stern, G.M. (1996) The BDNF content of postnatal and adult rat brain: the effects of 6-hydroxydopamine lesions in adult brain. Brain Res. Dev. Brain Res., 97, 297-303.