Simultaneous intrastriatal and intranigral grafting (double grafts) in the rat model of Parkinson's disease

Brain Research Reviews

Volumn 32, Issue 1, 2000, Pages 328-339

  Mendez, I ^a,b   Baker, K A ^a   Hong, M ^b  

^a Neural Transplantation Laboratory   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Intranigral grafting; Intrastriatal grafting; Parkinson's disease

Indexed keywords

FLUOROGOLD; TRACER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BEHAVIOR; CELL TRANSPLANTATION; DOPAMINERGIC SYSTEM; FEMALE; IMMUNOHISTOCHEMISTRY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SHORT SURVEY; SUBSTANTIA NIGRA;

EID: 0034030456     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-0173(99)00091-0     Document Type: Review

References (82)

1. Abercrombie M. Estimation of nuclear population from microtome sections. Anat. Rec. 94:1946;239-247.
2. Apostolides C., Sandford E., Hong M., Mendez I. Glial cell line-derived neurotrophic factor improves intrastriatal graft survival of stored dopaminergic cells. Neuroscience. 83:1998;363-372.
3. Björklund A., Schmidt R.H., Stenevi U. Functional reinnervation of the neostriatum in the adult rat by use of intraparenchymal grafting from the substantia nigra. Cell Tissue Res. 212:1980;39-45.
4. Bolam J.P., Freund T.F., Björklund A., Dunnett S.B., Smith A.D. Synaptic input and local output of dopaminergic neurons in grafts that functionally reinnervate the host neostriatum. Exp. Brain Res. 68:1987;131-146.
5. Cadelli D.S., Schwab M.E. Myelin-associated inhibitors of neurite outgrowth and their role in CNS regeneration. Ann. N.Y. Acad. Sci. 633:1991;234-240.
6. Campbell G.A., Eckardt M.J., Weight F.F. Dopaminergic mechanisms in subthalamic nucleus of rat: analysis using horseradish peroxidase and microiontophoresis. Brain Res. 333:1985;261-270.
7. Cheramy A., Leviel V., Glowinski J. Dendritic release of dopamine in the substantia nigra. Nature. 289:1981;537-542.
8. Cheramy A., Nieoullon A., Glowinski J. In vivo evidence for a dendritic release of dopamine in cat substantia nigra. Appl. Neurophysiol. 42:1979;57-59.
9. Clarke D.J., Brundin P., Strecker R.E., Nilsson O.G., Björklund A. Human fetal dopamine neurons grafted in a rat model of Parkinson's disease: ultrastructural evidence for synapse formation using tyrosine hydroxylase immunocytochemistry. Exp. Brain Res. 73:1988;115-126.
10. Denis-Donini S., Glowinski J., Prochiantz A. Specific influence of striatal target neurons on the in vitro outgrowth of mesencephalic dopaminergic neurites: a morphological qualitative study. Neuroscience. 3:1983;2292-2299.
11. Doucet G., Murata Y., Brundin P., Bosler O., Mons N., Geffard M., Ouimet C.C., Björklund A. Host afferents into intrastriatal transplants of fetal ventral mesencephalon. Exp. Neurol. 106:1989;1-19.
12. Dunnett S.B., Björklund A. Mechanisms of function of neural grafts in the adult mammalian brain. J. Exp. Biol. 132:1987;265-289.
13. Dunnett S.B., Roger D.C., Richards S.J. Nigrostriatal reconstruction after 6-OHDA lesions in rats: combination of dopamine-rich nigral grafts and nigrostriatal "bridge" grafts. Exp. Brain Res. 75:1989;523-535.
14. Fine A., Gaudet P., Holness R., King D., Fisk J., Lang A., Snow B., Heffernan L., Poirier R., Redman R., Hosokawa T., Leopold C., Mackay-Lyons M., Robertson H., Fingerhut F., Calne D. Fetal dopaminergic neural transplantation for treatment of Parkinson's disease: outcome after one year. Can. J. Neurol. Sci. 21(S2):1994;S27.
15. Floeter M.K., Jones E.J. Connections made by transplants to the cerebral cortex of rat brains damaged in utero. J. Neurosci. 4:1984;141-150.
16. Flores G., Valencia J., Rosales M.G., Sierra A., Aceves J. Appearance of EMG activity and motor asymmetry after unilateral lesions of the dopaminergic innervation to the subthalamic nucleus in the rat. Neurosci. Lett. 162:1993;153-156.
17. Freed C.R., Breeze R.E., Rosenberg N.L., Schneck S.A., Kriek E., Qi J.X., Lone T., Zhang Y.B., Snyder J.A., Wells T.H., Ramig L.O., Thomson L., Mazziotta J.C., Huang S.C., Grafton S.T., Brooks D., Sawle G., Schroter G., Ansari A.A. Survival of implanted fetal dopamine cells and improvement 12 to 46 months after transplantation for Parkinson's disease. New Engl. J. Med. 327:1992;1549-1555.
18. Freeman T.B., Olanow C.W., Hauser R.A., Nauert G.M., Smith D.A., Borlongan C.V., Sanberg P.R., Holt D.A., Kordower J.H., Vingerhoets F.J., Snow B.J., Calne D., Ganger L.L. Bilateral fetal nigral transplantation into the postcommissural putamen in Parkinson's disease. Ann. Neurol. 38:1995;379-388.
19. Freund T.F., Bolam J.P., Björklund A., Stenevi U., Dunnett S.B., Powell J.F., Smith A.D. Efferent synaptic connections of grafted dopaminergic neurons reinnervating the host neostriatum: a tyrosine hydroxylase immunocytochemical study. J. Neurosci. 5:1985;603-616.
20. Granholm A.C., Mott J.L., Bowenkamp K., Eken S., Henry S., Hoffer B.J., Lapchak P.A., Palmer M.R., van Horne C., Gerhardt G.A. Glial cell line-derived neurotrophic factor improves survival of ventral mesencephalic grafts to the 6-hydroxydopamine lesioned striatum. Exp. Brain Res. 116:1997;29-38.
21. Hassani O.K., François C., Yelnik J., Féger J. Evidence for a dopaminergic innervation of the subthalamic nucleus in the rat. Brain Res. 749:1997;88-94.
22. Herman J.P., Abrous D.N., Le M.M. Anatomical and behavioural comparison of unilateral dopamine-rich grafts implanted into the striatum of neonatal and adult rats. Neuroscience. 40:1991;465-475.
23. Ho A., Gore A.C., Weickert C.S., Blum M. Glutamate regulation of GDNF gene expression in the striatum and primary striatal astrocytes. NeuroReport. 6:1995;1454-1458.
24. Humpel C., Hoffer B., Strömberg I., Bektesh S., Collins F., Olson L. Neurons of the hippocampal formation express glial cell line-derived neurotrophic factor messenger RNA in response to kainate-induced excitation. Neuroscience. 59:1994;791-795.
25. Kopyov O.V., Jacques D.S., Lieberman A., Duma C.M., Rogers R.L. Outcome following intrastriatal fetal mesencephalic grafts for Parkinson's patients is directly related to the volume of grafted tissue. Exp. Neurol. 146:1997;536-545.
26. Kordower J.H., Freeman T.B., Chen E.Y., Mufson E.J., Sanberg P.R., Hauser R.A., Snow B., Olanow C.W. Fetal nigral grafts survive and mediate clinical benefit in a patient with Parkinson's disease. Mov. Disord. 13:1998;383-393.
27. Kordower J.H., Freeman T.B., Snow B.J., Vingerhoets F.J., Mufson E.J., Sanberg P.R., Hauser R.A., Smith D.A., Nauert G.M., Perl D.P., Olanow C.W. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. New Engl. J. Med. 332:1995;1118-1124.
28. Kordower J.H., Rosenstein J.M., Collier T.J., Burke M.A., Chen E.Y., Li J.M., Martel L., Levey A.E., Mufson E.J., Freeman T.B., Olanow C.W. Functional fetal nigral grafts in a patient with Parkinson's disease: chemoanatomic, ultrastructural, and metabolic studies. J. Comp. Neurol. 370:1996;203-230.
29. Lavoie B., Smith Y., Parent A. Dopaminergic innervation of the basal ganglia in the squirrel monkey as revealed by tyrosine hydroxylase immunohistochemistry. J. Comp. Neurol. 289:1989;36-52.
30. Levivier M., Dethy S., Rodesch F., Peschanski M., Vandesteene A., David P., Wikler D., Goldman S., Claes T., Biver F., Liesnard C., Goldman M., Hildebrand J., Brotchi J. Intracerebral transplantation of fetal ventral mesencephalon for patients with advanced Parkinson's disease. Methodology and 6-month to 1-year follow-up in 3 patients. Stereotact. Funct. Neurosurg. 69:1997;99-111.
31. Lindvall O. Update on fetal transplantation: the Swedish experience. Mov. Disord. 13(suppl1):1998;83-87.
32. Lindvall O., Björklund A. Dopaminergic innervation of the globus pallidus by collaterals from the nigrostriatal pathway. Brain Res. 172:1979;169-173.
33. Lindvall O., Brundin P., Widner H., Rehncrona S., Gustavii B., Frackowiak R., Leenders K.L., Sawle G., Rothwell J.C., Marsden C.D., Björklund A. Grafts of fetal dopamine neurons survive and improve motor function in Parkinson's disease. Science. 247:1990;574-577.
34. Lindvall O., Rehncrona S., Brundin P., Gustavii B., Åstedt B., Widner H., Lindholm T., Björklund A., Leenders K.L., Rothwell J.C., Frackowiak R., Marsden C.D., Johnels B., Steg G., Freedman R., Hoffer B.J., Seiger Å., Bygdeman M., Strömberg I., Olson L. Human fetal dopamine neurons grafted into striatum in two patients with severe Parkinson's disease. A detailed account of methodology and a 6-month follow-up. Arch. Neurol. 46:1989;615-631.
35. Lindvall O., Sawle G., Widner H., Rothwell J.C., Björklund A., Brooks D., Brundin P., Frackowiak R., Marsden C.D., Odin P., Rehncrona S. Evidence for long-term survival and function of dopaminergic grafts in progressive Parkinson's disease. Ann. Neurol. 35:1994;172-180.
36. Lindvall O., Widner H., Rehncrona S., Brundin P., Odin P., Gustavii B., Frackowiak R., Leenders K.L., Sawle G., Rothwell J.C., Björklund A., Marsden C.D. Transplantation of fetal dopamine neurons in Parkinson's disease: one-year clinical and and neurophysiological observations in two patients with putaminal implants. Ann. Neurol. 31:1992;155-165.
37. Clinica Puerta de Hierro Neural Transplantation Group, Lopez-Lozano J.J., Bravo G., Brera B., Millán I., Dargallo J., Salmeán J., Uría J., Insausti J. Long-term improvement in patients with severe Parkinson's disease after implantation of fetal ventral mesencephalic tissue in a cavity of the caudate nucleus: 5-year follow up in 10 patients. J. Neurosurg. 86:1997;931-942.
38. R.D. Lund, J.D. Radel, M.H. Hankin, H. Klassen, P.J. Coffey, J.N.P. Rawlins, Developmental and functional integrations of retinal transplants with host rat brains. In: A. Björklund, A.J. Aguayo, D. Ottoson (Eds.), Brain Repair, MacMillan, London, 1990, pp. 327-340.
39. Martin L.P., Waszczak B.L. D1 agonist-induced excitation of substantia nigra pars reticulata neurons: mediation by D1 dopamine receptors of striatonigral terminals via a pertussis toxin-sensitive coupling pathway. J. Neurosci. 14:1994;4494-4506.
40. Mehta V., Spears J., Mendez I. Neural transplantation in Parkinson's disease. Can. J. Neurol. Sci. 24:1997;292-301.
41. Mendez I., Elisevich K., Flumerfelt B. Dopaminergic innervation of substance P-containing striatal neurons by fetal nigral grafts: an ultrastructural double-labeling immunocytochemical study. J. Comp. Neurol. 308:1991;66-78.
42. Mendez I., Hong M. Reconstruction of the striato-nigro-striatal circuitry by simultaneous double dopaminergic grafts: a tracer study using fluorogold and horseradish peroxidase. Brain Res. 778:1997;194-205.
43. Mendez I., Sadi D., Hong M. Reconstruction of the nigrostriatal pathway by simultaneous intrastriatal and intranigral dopaminergic transplants. J. Neurosci. 16:1996;7216-7227.
44. 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.
45. Nikkhah G., Cunningham M.G., Cenci M.A., McKay R., Björklund A. Dopaminergic transplants into the substantia nigra of neonatal rats with bilateral 6-OHDA lesions. I. Evidence for anatomical reconstruction of the nigrostriatal pathway. J. Neurosci. 15:1995;3548-3561.
46. Nikkhah G., Cunningham M.G., Jödicke A., Knappe U., Björklund A. Improved graft survival and striatal reinnervation by microtransplantation of fetal nigral cell suspensions in the rat Parkinson model. Brain Res. 633:1994;133-143.
47. Nikkhah G., Cunningham M.G., McKay R., Björklund A. Dopaminergic transplants into the substantia nigra of neonatal rats with bilateral 6-OHDA lesions. II. Transplant-induced behavioural recovery. J. Neurosci. 15:1995;3562-3570.
48. 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.
49. Olanow C.W., Kordower J.H., Freeman T.B.et al. Fetal nigral transplantation as a therapy for Parkinson's disease. Trends Neurosci. 19:1996;102-109.
50. 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.
51. Parent A., Smith Y. Differential dopaminergic innervation of the two pallidal segments in the squirrel monkey (Saimiri sciureus). Brain Res. 426:1987;397-400.
52. Peschanski M., Defer G., N'Guyen J.P., Ricolfi F., Monfort J.C., Remy P., Geny C., Samson Y., Hantraye P., Jeny R., Gaston A., Kéravel Y., Degos J.D., Cesaro P. Bilateral motor improvement and alteration of L-dopa effect in two patients with Parkinson's disease following intrastriatal transplantation of foetal ventral mesencephalon. Brain. 117:1994;487-499.
53. Prochiantz A., DiPorzio U., Kato A., Berger B., Glowinski J. In vitro maturation of mesencephalic dopaminergic neurons from mouse embryos is enhanced in the presence of their striatal target cells. Proc. Natl. Acad. Sci. U.S.A. 76:1979;5387-5391.
54. Raineteau O., Z'Graggen W.J., Thallmair M., Schwab M.E. Sprouting and regeneration after pyramidotomy and blockade of the myelin-associated neurite growth inhibitors NI35/250 in adult rats. Eur. J. Neurosci. 11:1999;1486-1490.
55. Rioux L., Gaudin D.P., Bui L.K., Grégoire L., DiPaolo T., Bédard P.J. Correlation of functional recovery after a 6-hydroxydopamine lesion with survival of grafted fetal neurons and release of dopamine in the striatum of the rat. Neuroscience. 40:1991;123-131.
56. Robertson H.A. Synergistic interactions of D1- and D2-selective dopamine agonists in animal models for Parkinson's disease: sites of action and implications for the pathogenesis of dyskinesias. Can. J. Neurol. Sci. 19:1992;147-152.
57. Rosenblad C., Martinez-Serrano A., Björklund A. Glial cell line-derived neurotrophic factor increases survival, growth and function of intrastriatal fetal nigral dopaminergic grafts. Neuroscience. 75:1996;979-985.
58. Ruffieux A., Schultz W. Dopaminergic activation of reticulata neurones in the substantia nigra. Nature. 285:1980;240-241.
59. Schnell L., Schwab M.E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature. 343:1990;269-272.
60. Schnell L., Schwab M.E. Sprouting and regeneration of lesioned corticospinal tract fibers in the adult rat spinal cord. Eur. J. Neurosci. 5:1993;1156-1171.
61. Schwab M.E. Myelin-associated inhibitors of neurite growth and regeneration in the CNS. Trends Neurosci. 13:1990;452-456.
62. Sinclair S.R., Svendsen C.N., Torres E.M., Martin D., Fawcett J.W., Dunnett S.B. GDNF enhances dopaminergic cell survival and fibre outgrowth in embryonic nigral grafts. NeuroReport. 7:1996;2547-2552.
63. Snyder-Keller A.M., Carder R.K., Lund R.D. Development of dopamine innervation and turning behaviour in dopamine-depleted infant rats receiving unilateral nigral transplants. Neuroscience. 30:1989;779-794.
64. Sortwell C.E., Collier T.J., Sladek J.R. Jr. Co-grafted embryonic striatum increases the survival of grafted embryonic dopamine neurons. J. Comp. Neurol. 399:1998;530-540.
65. Spencer D.D., Robbins R.J., Naftolin F., Marek K.L., Vollmer T., Leranth C., Roth R.H., Price L.H., Gjedde A., Bunney B.S., Sass K.J., Elsworth J.D., Kier L., Makuch R., Hoffer P.B., Redmond D.E. Jr. Unilateral transplantation of human fetal mesencephalic tissue into the caudate nucleus of patients with Parkinson's disease. New Engl. J. Med. 327:1992;1541-1548.
66. Spenger C., Hyman C., Studer L., Egli M., Evtouchenko L., Jackson C., Dahl-Jorgenson A., Lindsay R.M., Seiler R.W. Effects of BDNF on dopaminergic, serotonergic and GABAergic neurons in cultures of human fetal ventral mesencephalon. Exp. Neurol. 133:1995;50-63.
67. Stanfield B.B., O'Leary D.D.M. Fetal occipital cortical neurones transplanted to the rostral cortex can extend and maintain a pyramidal tract axon. Nature. 313:1985;135-137.
68. Strömberg I., Björklund L., Johansson M., Tomac A., Collins F., Olson L., Hoffer B., Humpel C. Glial cell line-derived neurotrophic factor is expressed in developing but not adult striatum and stimulates developing dopamine neurons in vivo. Exp. Neurol. 124:1993;401-412.
69. Strömberg I., Humpel C. Expression of BDNF and trkB mRNAs in comparison to dopamine D1 and D2 receptor mRNAs and tyrosine hydroxylase-immunoreactivity in nigrostriatal in oculo co-grafts. Brain Res., Dev. Brain Res. 84:1995;215-224.
70. Tang F.I., Tien L.T., Zhou F.C., Hoffer B.J., Wang Y. Intranigral ventral mesencephalic grafts and nigrostriatal injections of glial cell line-derived neurotrophic factor restore dopamine release in the striatum of 6-hydroxydopamine-lesioned rats. Exp. Brain Res. 119:1998;287-296.
71. Wang Y., Tien L.T., Lapchak P.A., Hoffer B.J. GDNF triggers fiber outgrowth of fetal ventral mesencephalic grafts from nigra to striatum in 6-OHDA lesioned rats. Cell Tissue Res. 286:1996;223-233.
72. Wenning G.K., Odin P., Morrish P., Rehncrona S., Widner H., Brundin P., Rothwell J.C., Brown R., Gustavii B., Hagell P., Jahanshahi M., Sawle G., Björklund A., Brooks D.J., Marsden C.D., Quinn N.P., Lindvall O. Short- and long-term survival and function of unilateral intrastriatal dopaminergic grafts in Parkinson's disease. Ann. Neurol. 42:1997;95-107.
73. Wictorin K., Brundin P., Gustavii B., Lindvall O., Björklund A. Reformation of long axon pathways in adult rat central nervous system by human forebrain neuroblasts. Nature. 347:1990;556-558.
74. Wictorin K., Brundin P., Sauer H., Lindvall O., Björklund A. Long distance directed axonal growth from human dopaminergic mesencephalic neuroblasts implanted along the nigrostriatal pathway in 6-hydroxydopamine lesioned adult rats. J. Comp. Neurol. 323:1992;475-494.
75. 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.
76. Wictorin K., Simberley R.B., Isacson O., Swanson L.W., Björklund A. Connectivity of striatal grafts implanted into the ibotenic acid-lesioned striatum. III. Efferent projecting graft neurons and their relation to host afferents within the grafts. Neuroscience. 30:1989;313-330.
77. Widner H., Tetrud J., Rehncrona S., Snow B., Brundin P., Gustavii B., Björklund A., Lindvall O., Langston J.W. Bilateral fetal mesencephalic grafting in two patients with Parkinsonism induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. New Engl. J. Med. 327:1992;1556-1563.
78. Wilby M.J., Sinclair S.R., Muir E.M., Zietlow R., Adcock K.H., Horellou P., Rogers J.H., Dunnett S.B., Fawcett J.W. A glial cell line-derived neurotrophic factor-secreting clone of the Schwann cell line SCTM41 enhances survival and fiber outgrowth from embryonic nigral neurons grafted to the striatum and lesioned substantia nigra. J. Neurosci. 19:1999;2301-2312.
79. Yurek D.M., Lu W., Hipkens S., Wiegand S.J. BDNF enhances functional reinnervation of the striatum by grafted fetal dopamine neurons. Exp. Neurol. 137:1996;105-118.
80. Zhou F.C., Buchwald N. Connectivities of the striatal grafts in adult rat brain: a rich afference but scant striatonigral efference. Brain Res. 504:1989;15-30.
81. Zhou F.C., Chiang Y.H. Excitochemical-induced bridging directs axonal growth of transplanted neurons to distal target. Cell Transplant. 4:1995;103-112.
82. Zhou F.C., Chiang Y.H., Wang Y. Constructing a new nigrostriatal pathway in the Parkinsonian model with bridged neural transplantation in substantia nigra. J. Neurosci. 16:1996;6965-6974.