Intranigral transplants of GABA-rich striatal tissue induce behavioral recovery in the rat Parkinson model and promote the effects obtained by intrastriatal dopaminergic transplants

Experimental Neurology

Volumn 155, Issue 2, 1999, Pages 165-186

  Winkler, Christian ^a,b   Bentlage, Claas ^b   Nikkhah, Guido ^b   Samii, Madjid ^b   Björklund, Anders ^a  

^a LUND UNIVERSITY   (Sweden)

^b NORDSTADT HOSPITAL   (Germany)

Author keywords

Behavior; Dopamine; GABA; Nigra; Parkinson's disease; Striatum; Transplantation

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; DOPAMINE; OXIDOPAMINE;

AKINESIA; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN GRAFT; BRAIN TRANSPLANTATION; CIRCLING BEHAVIOR; COORDINATION; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; ENTOPEDUNCULAR NUCLEUS; FETAL TISSUE TRANSPLANTATION; IMMUNOHISTOCHEMISTRY; MESENCEPHALON; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SUBSTANTIA NIGRA;

EID: 0033054208     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1998.6916     Document Type: Article

References (56)

1. Abercrombie M. Estimation of nuclear population from microtome sections. Anat. Rec. 94:1946;239-247.
2. Anderson K. D., Reiner A. Immunohistochemical localization of DARPP-32 in striatal projection neurons and striatal interneurons: implications for the localization of D1-like dopamine receptors on different types of striatal neurons. Brain Res. 568:1991;235-243.
3. Bal A., Savasta M., Chritin M., Mennicken F., Abrous D. N., Le Moal M., Feuerstein C., Herman J. P. Transplantation of fetal nigral cells reverses the increase of preproenkephalin mRNA levels in the rat striatum caused by 6-OHDA lesion of the dopaminergic nigrostriatal pathway: a quantitative in situ hybridization study. Mol. Brain Res. 18:1993;221-227.
4. Bejjani B., Damier P., Arnulf I., Bonnet A. M., Vidailhet M., Dormont D., Pidoux B., Cornu P., Marsault C., Agid Y. Pallidal stimulation for Parkinson's disease: two targets. Neurology. 49:1997;1564-1569.
5. Björklund A. Dopaminergic transplants in experimental parkinsonism: Cellular mechanisms of graft-induced functional recovery. Curr. Opin. Neurobiol. 2:1992;683-689.
6. Björklund A., Dunnett S. B. Neural transplantation in adult rats. Neural Transplantation: A Practical Approach. 1992;Oxford Univ. Press, Oxford. p. 57-78.
7. Björklund A., Dunnett S. B., Nikkhah G. Nigral transplants in the rat Parkinson model: Functional limitations and strategies to enhance nigrostriatal reconstruction. Dunnett S. B., Björklund A. Functional Neural Transplantation. 1994;47-68 Raven Press, New York.
8. Björklund A., Lindvall O., Isacson O., Brundin P., Wictorin K., Strecker R. E., Clarke D. J., Dunnett S. B. Mechanisms of action of intracerebral neural implants. Trends Neurosci. 10:1987;509-516.
9. Björklund A., Lindvall O. Dopamine-containing systems in the CNS. örklund A. Bj, Hökfelt T. Handbook of Chemical Neuroanatomy. Vol 2. Classical Transmitters in the CNS. 1984;55-122 Elsevier, Amsterdam.
10. Björklund A., Stenevi U., Schmidt R. H., Dunnett S. B., Gage F. H. Intracerebral grafting of neuronal cell suspensions. I. Introduction and general methods of preparation. Acta Physiol. Scand. 522:1983;1-7.
11. Campbell K., Kalén P., Wictorin K., Lundberg C., Mandel R. J., Björklund A. Characterization of GABA release from intrastriatal striatal transplants: Dependence on host-derived afferents. Neuroscience. 53:1993;403-415.
12. Campbell K., Wictorin K., Björklund A. Neurotransmitter-related gene expression in intrastriatal striatal transplants. I. Phenotypical characterization of striatal and non-striatal graft regions. Neuroscience. 64:1995;17-33.
13. Cenci M. A., Kalén P., Mandel R. J., Wictorin K., Björklund A. Dopaminergic transplants normalize amphetamine- and apomorphine-induced Fos expression the 6-hydroxydopamine-lesioned striatum. Neuroscience. 46:1992;943-957.
14. Cenci M. A., Campbell K., Björklund A. Neuropeptide messenger RNA expression in the 6-hydroxydopamine-lesioned rat striatum reinnervated by fetal dopaminergic transplants: Differential effects of the grafts on preproenkephalin, preprotachykinin and prodynorphin messenger RNA levels. Neuroscience. 57:1993;275-296.
15. Chesselet M. F., Delfs J. M. Basal ganglia and movement disorders: an update. Trends Neurosci. 19:1996;417-422.
16. Chevalier G., Deniau J. M. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 13:1990;277-280.
17. Doucet G., Brundin P., Descarries L., Björklund A. Effect of prior dopamine denervation on survival and fiber outgrowth from intrastriatal fetal mesencephalic grafts. Eur. J. Neurosci. 2:1990;279-290.
18. Dunnett S. B., Björklund A. Staging and dissection of rat embryos. Dunnett S. B., Björklund A. Neural Transplantation: A Practical Approach. 1992;1-18 Oxford Univ. Press, Oxford.
19. Dunnett S. B., Björklund A., Schmidt R. H., Stenevi U., Iversen S. D. Intracerebral grafting of neuronal cell suspensions. IV. Behavioural recovery in rats with unilateral 6-OHDA lesions following implantation of nigral cell suspensions in different forebrain sites. Acta Physiol. Scand. 522:1983;29-37.
20. Dunnett S. B., Björklund A., Stenevi U., Iversen S. D. Grafts of embryonic substantia nigra reinnervating the ventrolateral striatum ameliorate sensorimotor impairments and akinesia in rats with 6-OHDA lesions of the nigrostriatal pathway. Brain Res. 229:1981;209-217.
21. Dunnett S. B., Whishaw I. Q., Rogers D. C., Jones G. H. Dopamine-rich grafts ameliorate whole body motor asymmetry and sensory neglect but not independent limb use in rats with 6-hydroxydopamine lesions. Brain Res. 415:1987;63-78.
22. German D. C., Schlusselberg D. S., Woodward D. J. Three-dimensional computer reconstruction of midbrain dopaminergic neuronal populations: from mouse to man. J. Neural Transm. 57:1983;243-254.
23. Graybiel A. M. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci. 13:1990;244-253.
24. Hemmings H. C. Jr., Greengard P. DARPP-32, a dopamine- and adenosine 3′,5′-monophosphate-regulated phosphoprotein: Regional, tissue, and phylogenetic distribution. J. Neurosci. 6:1986;1469-1481.
25. Herman J. P., Abrous D. N. Dopaminergic neural grafts after fifteen years: results and perspectives. Prog. Neurobiol. 44:1994;1-35.
26. Janson A. M., Møller A. Chronic nicotine treatment counteracts nigral cell loss induced by a partial mesondiencephalic hemitransection: An analysis of total number and mean volume of neurons and glia in substantia nigra in the rat. Neuroscience. 57:1993;931-941.
27. Kirik D., Rosenblad C., Björklund A. Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Exp. Neurol. 152:1998;259-277.
28. Laitinen L. V., Bergenheim A. T., Hariz M. I. Leksell's posteroventral pallodotomy in the treatment of Parkinson's disease. J. Neurosurg. 76:1992;53-61.
29. Limousin P., Greene J., Pollak P., Rothwell J., Benabid A. L., Frackowiak R. Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson's disease. Ann. Neurol. 42:1997;283-291.
30. Limousin P., Pollak P., Benazzouz A., Hoffmann D., Le Bas J. F., Broussolle E., Perret J. E., Benabid A. L. Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet. 345:1995;91-95.
31. Mandel R. J., Brundin P., Björklund A. The importance of graft placement and task complexity for transplant-induced recovery of simple and complex sensorimotor deficits in dopamine denervated rats. Eur. J. Neurosci. 2:1990;888-894.
32. Manier M., Abrous D. N., Feuerstein C., Le Moal M., Herman J. P. Increase of striatal methionin enkephalin content following lesion of the nigrostriatal dopaminergic pathway in adult rats and reversal following the implantation of embryonic dopaminergic neurons: A quantitative immunohistochemical analysis. Neuroscience. 42:1991;427-439.
33. Marsden C. D., Obeso J. A. The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson′s disease. Brain. 117:1994;877-897.
34. Mendez I., Naus C. C. G., Elisevitch K., Flumerfeld B. A. Normalization of striatal proenkephalin and preprotachykinin mRNA expression by fetal substantia nigra grafts. Exp. Neurol. 119:1993;1-10.
35. Mendez I., Sadi D., Hong M. Reconstruction of the nigrostriatal pathway by simultaneous intrastriatal and intranigral dopaminergic transplants. J. Neurosci. 16:1996;7216-7227.
36. 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. Methods. 36:1991;219-228.
37. Nakao N., Ogura M., Nakai K., Itakura T. Intrastriatal mesencephalic grafts affect neuronal activity in basal ganglia nuclei and their target structures in a rat model of Parkinson's disease. J. Neurosci. 18:1998;1806-1817.
38. Nikkhah G., Duan W. M., Knappe U., Jödicke A., Björklund A. Restoration of complex sensorimotor behavior and skilled forelimb use by a modified nigral cell suspension transplantation approach in the rat Parkinson model. Neuroscience. 56:1993;33-43.
39. Nikkhah G., Bentlage C., Cunningham M. G., Björklund A. Intranigral fetal dopamine grafts induce behavioral compensation in the rat Parkinson model. J. Neurosci. 14:1994;3449-3461.
40. Nikkhah G., Cunningham M. G., Jödicke A., Knappe U., Björklund A. Improved graft survival and striatal reinnervation using an microtransplantation approach in the rat Parkinson model. Brain Res. 633:1994;133-143.
41. Nikkhah G., Olsson M., Eberhard J., Bentlage C., Cunningham M. G., Björklund A. A microtransplantation approach for cell suspension grafting in the rat Parkinson model: A detailed account of the methodology. Neuroscience. 63:1994;57-72.
42. Olsson M., Nikkhah G., Bentlage C., Björklund 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.
43. Parent A., Hazrati L. N. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res. Rev. 20:1995;128-154.
44. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 1997;Academic Press, San Diego.
45. Robertson H. A. Dopamine receptor interactions: Some implications for the treatment of Parkinson's disease. Trends Neurosci. 15:1992;201-206.
46. Schallert T., De Ryck M., Whishaw I. Q., Ramirez V. D., Teitelbaum P. Excessive bracing reactions and their control by atropine andl. Exp. Neurol. 64:1979;33-43.
47. Schallert T., Hall S. 'Disengage' sensorimotor deficit following apparent recovery from unilateral dopamine depletion. Behav. Brain Res. 30:1988;15-24.
48. Schallert T., Norton D., Jones T. A. A clinically relevant unilateral rat model of parkinsonian akinesia. J. Neural Transplant. Plast. 3:1992;332-333.
49. Siegfried J., Lippitz B. Bilateral chronic electrostimulation of ventroposterolateral pallidum: A new therapeutic approach for alleviating all parkinsonian symptoms. Neurosurgery. 35:1994;1126-1129.
50. Sirinathsinghji D. J. S., Dunnett S. B. Increased proenkephalin mRNA levels in the rat neostriatum following lesion of the ipsilateral nigrostriatal dopamine pathway with 1-methyl-4-phenylpyridinium ion (MPP(+)): Reversal by embryonic nigral dopamine grafts. Mol. Brain Res. 9:1991;263-269.
51. Ungerstedt U., Arbuthnott G. Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res. 24:1970;485-493.
52. Wichmann T., DeLong M. R. Pathophysiology of parkinsonian motor abnormalities. Adv. Neurol. 60:1993;53-61.
53. Wictorin K., Ouimet C. C., Björklund A. Intrinsic organization and connectivity of intrastriatal striatal transplants in rats as revealed by DARPP-32 immunohistochemistry: Specificity of connections with the lesioned host brain. Eur. J. Neurosci. 1:1989;690-701.
54. Winkler C., Sauer H., Lee C. S., Björklund 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.
55. Winkler C. Eur. J. Neurosci. 10:1998;118.17.
56. Yurek D. M. Intranigral transplants of fetal ventral mesencephalic tissue attenuate D1-agonist-induced rotational behavior. Exp. Neurol. 143:1997;1-9.