Differential vulnerability of primate caudate-putamen and striosome-matrix dopamine systems to the neurotoxic effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (original) (raw)

Abstract

The meperidine analogue derivative 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) induces nigrostriatal fiber damage and severe parkinsonism in humans and animals. MPTP-induced parkinsonism has been proposed as a model of Parkinson disease, but doubts have been raised about whether the patterns of nigrostriatal fiber loss in the two conditions are similar. We report here observations on [3H]mazindol monoamine (principally dopamine) uptake-site binding in the striatum of monkeys (Saimiri sciureus) exposed to low doses of MPTP. We show that this treatment can produce a pattern of nigrostriatal degeneration characteristic of that seen in Parkinson disease, in which there is greater depletion of dopaminergic markers in the putamen than in the caudate nucleus, especially posteriorly. Moreover, within the regions of diminished uptake-site binding in the MPTP-treated monkeys, there is differential preservation of binding in striosomes relative to the surrounding matrix. We suggest that both regional and striosome/matrix patterns of nigrostriatal depletion are key features of MPTP-induced neurodegeneration and that both patterns may provide clues to the mechanisms underlying neurodegeneration in Parkinson disease as well.

3859

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Brooks D. J., Ibanez V., Sawle G. V., Quinn N., Lees A. J., Mathias C. J., Bannister R., Marsden C. D., Frackowiak R. S. Differing patterns of striatal 18F-dopa uptake in Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy. Ann Neurol. 1990 Oct;28(4):547–555. doi: 10.1002/ana.410280412. [DOI] [PubMed] [Google Scholar]
  2. Calne D. B., Langston J. W. Aetiology of Parkinson's disease. Lancet. 1983 Dec 24;2(8365-66):1457–1459. doi: 10.1016/s0140-6736(83)90802-4. [DOI] [PubMed] [Google Scholar]
  3. Davis G. C., Williams A. C., Markey S. P., Ebert M. H., Caine E. D., Reichert C. M., Kopin I. J. Chronic Parkinsonism secondary to intravenous injection of meperidine analogues. Psychiatry Res. 1979 Dec;1(3):249–254. doi: 10.1016/0165-1781(79)90006-4. [DOI] [PubMed] [Google Scholar]
  4. Eidelberg E., Brooks B. A., Morgan W. W., Walden J. G., Kokemoor R. H. Variability and functional recovery in the N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of parkinsonism in monkeys. Neuroscience. 1986 Aug;18(4):817–822. doi: 10.1016/0306-4522(86)90102-8. [DOI] [PubMed] [Google Scholar]
  5. Elsworth J. D., Deutch A. Y., Redmond D. E., Jr, Taylor J. R., Sladek J. R., Jr, Roth R. H. Symptomatic and asymptomatic 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primates: biochemical changes in striatal regions. Neuroscience. 1989;33(2):323–331. doi: 10.1016/0306-4522(89)90212-1. [DOI] [PubMed] [Google Scholar]
  6. Flaherty A. W., Graybiel A. M. Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations. J Neurophysiol. 1991 Oct;66(4):1249–1263. doi: 10.1152/jn.1991.66.4.1249. [DOI] [PubMed] [Google Scholar]
  7. Garnett E. S., Lang A. E., Chirakal R., Firnau G., Nahmias C. A rostrocaudal gradient for aromatic acid decarboxylase in the human striatum. Can J Neurol Sci. 1987 Aug;14(3 Suppl):444–447. doi: 10.1017/s0317167100037884. [DOI] [PubMed] [Google Scholar]
  8. German D. C., Dubach M., Askari S., Speciale S. G., Bowden D. M. 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonian syndrome in Macaca fascicularis: which midbrain dopaminergic neurons are lost? Neuroscience. 1988 Jan;24(1):161–174. doi: 10.1016/0306-4522(88)90320-x. [DOI] [PubMed] [Google Scholar]
  9. Gibb W. R., Terruli M., Lees A. J., Jenner P., Marsden C. D. The evolution and distribution of morphological changes in the nervous system of the common marmoset following the acute administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Mov Disord. 1989;4(1):53–74. doi: 10.1002/mds.870040109. [DOI] [PubMed] [Google Scholar]
  10. Graybiel A. M., Hirsch E. C., Agid Y. The nigrostriatal system in Parkinson's disease. Adv Neurol. 1990;53:17–29. [PubMed] [Google Scholar]
  11. Graybiel A. M., Moratalla R. Dopamine uptake sites in the striatum are distributed differentially in striosome and matrix compartments. Proc Natl Acad Sci U S A. 1989 Nov;86(22):9020–9024. doi: 10.1073/pnas.86.22.9020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Graybiel A. M. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci. 1990 Jul;13(7):244–254. doi: 10.1016/0166-2236(90)90104-i. [DOI] [PubMed] [Google Scholar]
  13. Graybiel A. M., Ragsdale C. W., Jr Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5723–5726. doi: 10.1073/pnas.75.11.5723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Herkenham M., Little M. D., Bankiewicz K., Yang S. C., Markey S. P., Johannessen J. N. Selective retention of MPP+ within the monoaminergic systems of the primate brain following MPTP administration: an in vivo autoradiographic study. Neuroscience. 1991;40(1):133–158. doi: 10.1016/0306-4522(91)90180-v. [DOI] [PubMed] [Google Scholar]
  15. Javitch J. A., Strittmatter S. M., Snyder S. H. Differential visualization of dopamine and norepinephrine uptake sites in rat brain using [3H]mazindol autoradiography. J Neurosci. 1985 Jun;5(6):1513–1521. doi: 10.1523/JNEUROSCI.05-06-01513.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jones E. G., Coulter J. D., Hendry S. H. Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J Comp Neurol. 1978 Sep 15;181(2):291–347. doi: 10.1002/cne.901810206. [DOI] [PubMed] [Google Scholar]
  17. Kaufman M. J., Madras B. K. Severe depletion of cocaine recognition sites associated with the dopamine transporter in Parkinson's-diseased striatum. Synapse. 1991 Sep;9(1):43–49. doi: 10.1002/syn.890090107. [DOI] [PubMed] [Google Scholar]
  18. Kish S. J., Shannak K., Hornykiewicz O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N Engl J Med. 1988 Apr 7;318(14):876–880. doi: 10.1056/NEJM198804073181402. [DOI] [PubMed] [Google Scholar]
  19. Kopin I. J., Markey S. P. MPTP toxicity: implications for research in Parkinson's disease. Annu Rev Neurosci. 1988;11:81–96. doi: 10.1146/annurev.ne.11.030188.000501. [DOI] [PubMed] [Google Scholar]
  20. Künzle H. Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res. 1975 May 2;88(2):195–209. doi: 10.1016/0006-8993(75)90384-4. [DOI] [PubMed] [Google Scholar]
  21. Langer L. F., Graybiel A. M. Distinct nigrostriatal projection systems innervate striosomes and matrix in the primate striatum. Brain Res. 1989 Oct 2;498(2):344–350. doi: 10.1016/0006-8993(89)91114-1. [DOI] [PubMed] [Google Scholar]
  22. Langston J. W., Ballard P., Tetrud J. W., Irwin I. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science. 1983 Feb 25;219(4587):979–980. doi: 10.1126/science.6823561. [DOI] [PubMed] [Google Scholar]
  23. Lowenstein P. R., Joyce J. N., Coyle J. T., Marshall J. F. Striosomal organization of cholinergic and dopaminergic uptake sites and cholinergic M1 receptors in the adult human striatum: a quantitative receptor autoradiographic study. Brain Res. 1990 Feb 26;510(1):122–126. doi: 10.1016/0006-8993(90)90736-u. [DOI] [PubMed] [Google Scholar]
  24. Marshall J. F., Navarrete R. J. Contrasting tissue factors predict heterogeneous striatal dopamine neurotoxicity after MPTP or methamphetamine treatment. Brain Res. 1990 Nov 26;534(1-2):348–351. doi: 10.1016/0006-8993(90)90156-6. [DOI] [PubMed] [Google Scholar]
  25. Pifl C., Schingnitz G., Hornykiewicz O. Effect of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine on the regional distribution of brain monoamines in the rhesus monkey. Neuroscience. 1991;44(3):591–605. doi: 10.1016/0306-4522(91)90080-8. [DOI] [PubMed] [Google Scholar]
  26. Pifl C., Schingnitz G., Hornykiewicz O. The neurotoxin MPTP does not reproduce in the rhesus monkey the interregional pattern of striatal dopamine loss typical of human idiopathic Parkinson's disease. Neurosci Lett. 1988 Oct 5;92(2):228–233. doi: 10.1016/0304-3940(88)90066-3. [DOI] [PubMed] [Google Scholar]
  27. Porrino L. J., Viola J. J., Crane A. M., Pontieri F. E. Alterations in opiate receptor binding in MPTP-induced hemiparkinsonian monkeys. Neurosci Lett. 1991 Jun 24;127(2):155–159. doi: 10.1016/0304-3940(91)90783-p. [DOI] [PubMed] [Google Scholar]
  28. Ragsdale C. W., Jr, Graybiel A. M. A simple ordering of neocortical areas established by the compartmental organization of their striatal projections. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6196–6199. doi: 10.1073/pnas.87.16.6196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Selemon L. D., Goldman-Rakic P. S. Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J Neurosci. 1985 Mar;5(3):776–794. doi: 10.1523/JNEUROSCI.05-03-00776.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shoffner J. M., Watts R. L., Juncos J. L., Torroni A., Wallace D. C. Mitochondrial oxidative phosphorylation defects in Parkinson's disease. Ann Neurol. 1991 Sep;30(3):332–339. doi: 10.1002/ana.410300304. [DOI] [PubMed] [Google Scholar]
  31. Snyder S. H., D'Amato R. J. MPTP: a neurotoxin relevant to the pathophysiology of Parkinson's disease. The 1985 George C. Cotzias lecture. Neurology. 1986 Feb;36(2):250–258. doi: 10.1212/wnl.36.2.250. [DOI] [PubMed] [Google Scholar]
  32. Tetrud J. W., Langston J. W. The effect of deprenyl (selegiline) on the natural history of Parkinson's disease. Science. 1989 Aug 4;245(4917):519–522. doi: 10.1126/science.2502843. [DOI] [PubMed] [Google Scholar]
  33. Turner B. H., Wilson J. S., McKenzie J. C., Richtand N. MPTP produces a pattern of nigrostriatal degeneration which coincides with the mosaic organization of the caudate nucleus. Brain Res. 1988 Nov 8;473(1):60–64. doi: 10.1016/0006-8993(88)90315-0. [DOI] [PubMed] [Google Scholar]
  34. Wilson J. S., Turner B. H., Morrow G. D., Hartman P. J. MPTP produces a mosaic-like pattern of terminal degeneration in the caudate nucleus of dog. Brain Res. 1987 Oct 13;423(1-2):329–332. doi: 10.1016/0006-8993(87)90857-2. [DOI] [PubMed] [Google Scholar]