Implantation of bioactive growth factor-secreting rods enhances fetal dopaminergic graft survival, outgrowth density, and functional recovery in a rat model of Parkinson's disease

Experimental Neurology

Volumn 164, Issue 1, 2000, Pages 130-138

  Törnqvist, Nina ^a   Björklund, Lars ^a   Almqvist, Per ^a   Wahlberg, Lars ^a   Strömberg, Ingrid ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Bioactive rods; Graft; Neurotrophic factors; Parkinson's disease; Substantia nigra

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; EPIDERMAL GROWTH FACTOR; GROWTH FACTOR; NEURITE PROMOTING FACTOR; NEUROTROPHIC FACTOR; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN GRAFT; CELL COUNT; CELL SURVIVAL; CIRCLING BEHAVIOR; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FETAL TISSUE TRANSPLANTATION; FETUS; GRAFT SURVIVAL; IMPLANTATION; INNERVATION; MESENCEPHALON; NERVE FIBER GROWTH; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SUBSTANTIA NIGRA;

EID: 0343517501     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.2000.7411     Document Type: Article

References (63)

1. Abercrombie M. Estimation of nuclear population from microtome sections. Anat. Rec. 94:1946;239-247.
2. Barbe M. F. Tempting fate and commitment in the developing forebrain. Neuron. 16:1996;1-4.
3. Barker R. A., Dunnett S. B., Faissner A., Fawcett J. W. The time course of loss of dopaminergic neurons and the gliotic reaction surrounding grafts of embryonic mesencephalon to the striatum. Exp. Neurol. 141:1996;79-93.
4. Bean A. J., Elde R., Cao Y., Oellig C., Tamminga C., Goldstein M., Pettersson R. F., Hökfelt T. Expression of acidic and basic fibroblast growth factors in the substantia nigra of rat, monkey and human. Proc. Natl. Acad. Sci. USA. 88:1991;10237-10241.
5. Beck K. D., Valverde J., Alexi T., Poulsen K., Moffat B., Vandlen R. A., Rosenthal A., Hefti F. Mesencephalic dopaminergic neurons protected by GDNF from axotomy-induced degeneration in the adult brain. Nature. 373:1995;339-341.
6. Björklund A., Stenevi U. Reconstruction of the nigrostriatal dopamine pathway by intracerebral nigral transplants. Brain Res. 177:1979;555-560.
7. Björklund L., Spenger C., Strömberg I. Tirilazad mesylate increases dopaminergic neuronal survival in the in oculo grafting model. Exp. Neurol. 148:1997;324-333.
8. Björklund L., Vidal N., Strömberg I. Lazaroid-enhanced survival of grafted dopamine neurons does not increase target innervation. NeuroReport. 9:1998;2815-2819.
9. 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 striatum. Exp. Brain Res. 68:1987;131-146.
10. Brundin P., Isacson O., Gage F., Björklund A. Intrastriatal grafting of dopamine-containing neuronal cell suspensions: Effects of mixing with target or non-target cells. Dev. Brain Res. 24:1986;77-84.
11. Cintra A., Cao Y., Oellig C., Tinner B., Bortolotti F., Goldstein M., Pettersson R., Fuxe K. Basic FGF is present in dopaminergic neurons of ventral midbrain of the rat. NeuroReport. 2:1991;597-600.
12. Costantini L. C., Vozza B. M., Snyder-Keller A. M. Enhanced efficacy of nigral-striatal cotransplants in bilaterally dopamine-depleted rats: An anatomical and behavioral analysis. Exp. Neurol. 127:1994;219-231.
13. De Beaurepaire R., Freed W. J. Embryonic substantia nigra grafts innervate embryonic striatal co-grafts in preference to mature host striatum. Exp. Neurol. 95:1987;448-454.
14. Emgård-Mattson M., Karlsson J., Nakao N., Brundin P. Addition of lateral ganglionic eminence to rat mesencephalic grafts affects fiber outgrowth but does not enhance function. Cell Transplant. 6:1997;277-286.
15. Fallon J. H., Seroogy K. B., Loughlin S. E., Morrison R. S., Bradshaw R. A., Knaver D. J., Cunningham D. D. Epidermal growth factor immunoreactive material in the central nervous system: Location and development. Science. 224:1984;1107-1109.
16. 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.
17. Gash D. M., Zhang Z., Cass W. A., Ovadia A., Simmerman L., Martin D., Russell D., Collins F., Hoffer B. J., Gerhardt G. A. Morphological and functional effects of intranigrally administered GDNF in normal rhesus monkeys. J. Comp. Neurol. 363:1995;345-358.
18. Gensburger C., Labourdette G., Sensenbrenner M. Brain basic fibroblast growth factor stimulates the proliferation of rat neuronal precursor cells in vitro. FEBS Lett. 217:1987;1-5.
19. Giacobini M. M. J., Strömberg I., Almström S., Cao Y., Olson L. Fibroblast growth factors enhance dopamine fiber formation from nigral grafts. Dev. Brain Res. 75:1993;65-73.
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. Grothe C., Zachmann K., Unsicker K. Basic FGF-like immunoreactivity in the developing and adult rat brainstem. J. Comp. Neurol. 305:1991;328-336.
22. Hoffman D., Wahlberg L., Aebischer P. NGF released from a polymer matrix prevents loss of ChAT expression in basal forebrain neurons following a fimbria-fornix lesion. Exp. Neurol. 110:1990;39-44.
23. Hudson J., Granholm A.-C., Gerhardt G. A., Henry M. A., Hoffman A., Biddle P., Leela N. S., Mackerlova L., Lile J. D., Collins F., Hoffer B. J. Glial cell line-derived neurotrophic factor augments midbrain dopaminergic circuits in vivo. Brain Res. Bull. 36:1995;425-432.
24. Jaeger C. B. Cytoarchitectonics of substantia nigra grafts: A light- and electronmicroscopic study of immunocytochemically identified dopaminergic neurons and fibrous astrocytes. J. Comp. Neurol. 231:1985;121-135.
25. Johansson M., Friedemann M., Hoffer B., Strömberg I. Effects of glial cell line-derived neurotrophic factor on developing and mature ventral mesencephalic grafts in oculo. Exp. Neurol. 134:1995;25-34.
26. Knusel B., Michel P. P., Schwaber J. S., Hefti F. Selective and nonselective stimulation of central cholinergic and dopaminergic development in vitro by nerve growth factor, basic fibroblast growth factor, epidermal growth factor, insulin and the insulin-like growth factors I and II. J. Neurosci. 10:1990;558-570.
27. Krieglstein K., Henheik P., Farkas L., Jaszi J., Galter D., Krohn K., Unsicker K. Glial cell line-derived neurotrophic factor requires transforming growth factor-beta for exerting its full neurotrophic potential on peripheral and CNS neurons. J. Neurosci. 18:1998;9822-9834.
28. Krieglstein K., Unsicker K. Transforming factor-β promotes survival of midbrain dopaminergic neurons and protects them against n-methyl-4-phenylpyridinium ion toxicity. Neuroscience. 63:1994;1189-1196.
29. Lendahl U., Zimmerman L. B., McKay R. D. G. CNS stem cells express a new class of intermediate filament protein. Cell. 60:1990;585-595.
30. Lin L.-F. H., Doherty D. H., Lile J. D., Bektesh S., Collins F. GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science. 260:1993;1130-1132.
31. Mahalik T. J., Finger T. E., Strömberg I., Olson L. Substantia nigra transplants into denervated striatum of the rat: Ultrastructure of graft and host interconnections. J. Comp. Neurol. 260:1985;60-70.
32. Mayer E., Fawcett J., Dunnett S. Basic fibroblast growth factor promotes the survival of embryonic ventral mesencephalic dopaminergic neurons: Effects on nigral transplants in vivo. Neuroscience. 56:1993;389-398.
33. Meyer M., Zimmer J., Seiler R. W., Widmer H. R. GDNF increases the density of cells containing calbindin but not of cells containing calretinin in cultured rat and human fetal nigral tissue. Cell Transplant. 8:1999;25-36.
34. Mogi M., Harada M., Kondo T., Narabayashi H., Riederer P., Nagatsu T. Transforming growth factor-β1 levels are elevated in the striatum and in ventricular cerebrospinal fluid in Parkinson's disease. Neurosci. Lett. 193:1995;129-132.
35. Morshead C. M., van der Koy D. Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult brain. J. Neurosci. 12:1992;249-256.
36. Murphy M., Drago J., Bartlett P. Fibroblast growth factor stimulates the proliferation and differentiation of neuronal precursor cells in vitro. J. Neurosci. Res. 25:1990;463-475.
37. Mytilineou C., Park T., Shen J. Epidermal growth factor-induced survival and proliferation of neuronal precursor cells from embryonic rat mesencephalon. Neurosci. Lett. 135:1992;62-66.
38. Nikkhah G., Cunningham M. G., Jödicke A., Knappe U., Björklund A. Improved survival and striatal reinnervation by microtransplantation of fetal nigral cell suspensions in the rat Parkinson model. Brain Res. 633:1994;133-143.
39. 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.
40. Perlow M. J., Freed W. J., Hoffer B. J., Seiger Å., Olson L., Wyatt R. J. Brain grafts reduce motor abnormalities produced by destruction of nigrostriatal dopamine system. Science. 204:1979;643-647.
41. Poulsen K. T., Armanini M. P., Klein R. D., Hynes M. A., Phillips H. S., Rosenthal A. TGFβ2 and TGFβ3 are potent survival factors for midbrain dopaminergic neurons. Neuron. 13:1994;1245-1252.
42. Ray J., Peterson D., Schinstine M., Gage F. Proliferation, differentiation, and long-term culture of primary hippocampal neurons. Proc. Natl. Acad. Sci. USA. 90:1993;3602-3606.
43. 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.
44. Santa-Olalla J., Covarrubias L. Epidermal growth factor (EGF), transforming growth factor-α (TGF-α), and basic fibroblast growth factor (bFGF) differentially influence neural precursor cells of mouse embryonic mesencephalon. J. Neurosci. Res. 42:1995;172-183.
45. Sautter J., Tseng J., Braguglia D., Aebischer P., Spenger C., Seiler R., Widmer H., Zurn A. Implants of polymer-encapsulated genetically modified cells releasing glial cell line-derived neurotrophic factor improve survival, growth, and function of fetal dopaminergic grafts. Exp. Neurol. 149:1998;230-236.
46. Seroogy K. B., Gall C. M., Lee D. C., Kornblum H. I. Proliferative zones of postnatal rat brain express epidermal growth factor receptor mRNA. Brain Res. 670:1995;157-164.
47. Seroogy K. B., Numan S., Gall C. M., Lee D. C., Kornblum H. I. Expression of EGF receptor mRNA in rat nigrostriatal system. NeuroReport. 6:1994;105-108.
48. Sladek J. R. Jr., Collier T. J., Elsworth J. D., Taylor J. R., Roth R. H., Redmond D. E. Jr. Can graft-derived neurotrophic activity be used to direct axonal outgrowth of grafted dopamine neurons for circuit reconstruction in primates? Exp. Neurol. 124:1993;134-139.
49. Strömberg I., Bickford P. Reduced aging effects of striatal neuronal discharge rate by aged ventral mesencephalic grafts. NeuroReport. 7:1996;693-696.
50. Strömberg I., Björklund L., Förander P. The age of striatum determines the pattern and extent of dopaminergic innervation: A nigrostriatal double graft study. Cell Transplant. 6:1997;287-296.
51. Strömberg I., Björklund L., Johansson M., Tomac A., Collins F., Olson L., Hoffer B., Humpel C. Glial cell-derived neurotrophic factor (GDNF) is expressed in the developing but not adult striatum and stimulates developing dopamine neurons in vivo. Exp. Neurol. 124:1993;401-412.
52. Strömberg I., Herrera-Marschitz M., Ungerstedt U., Ebendal T., Olson L. Chronic implants of chromaffin tissue into the dopamine-denervated striatum: Effects of NGF on graft survival, fiber growth and rotational behavior. Exp. Brain Res. 60:1985;335-349.
53. Studer L., Tabar V., McKay R. D. G. Transplantation of expanded mesencephalic precursors leads to recovery in parkinsonian rats. Nature Neurosci. 1:1998;290-295.
54. Tomac A., Lindqvist E., Lin L.-F., Ögren S. O., Young D., Hoffer B. J., Olson L. Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature. 373:1995;335-339.
55. Unsicker K., Flanders K., Cissel D. S., Lafyatis R., Sporn M. B. Transforming growth factor beta isoforms in the adult rat central and peripheral nervous system. Neuroscience. 44:1991;613-625.
56. Varon S., Peterson G. M., Wictorin K., Fischer W., Björklund A., Gage F. H. Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc. Natl. Acad. Sci. USA. 83:1986;9231-9235.
57. Vawter M. P., Dillon-Carter O., Tourtellotte W. W., Carvey P., Freed W. J. TGFβ1 and TGFβ2 concentrations are elevated in Parkinson's disease in ventricular cerebrospinal fluid. Exp. Neurol. 142:1996;313-322.
58. Vidal N., Björklund L., Strömberg I. Morphological and functional evidence for enhanced growth and potassium-evoked dopamine release in striatal grafts innervated with a patchy growth pattern: An in oculo nigrostriatal cograft study. Cell Transplant. 7:1998;1-12.
59. Wahlberg L. Implantable Bioartificial Hybrids for Targeted Therapy in the Central Nervous System. 1997;Karolinska Institute, Stockholm.
60. Wanaka A., Milbrandt J., Johnson E. Expression of FGF receptor gene in rat development. Development. 111:1991;455-468.
61. 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 to the lesioned substantia nigra. J. Neurosci. 19:1999;2301-2312.
62. Yurek D. M., Collier T. J., Sladek J. R. Jr. Embryonic mesencephalic and striatal co-grafts: Development of grafted dopamine neurons and functional recovery. Exp. Neurol. 109:1990;191-199.
63. Zawada M. W., Zastrow D. J., Clarkson E. D., Adams F. S., Bell K. P., Freed C. R. Growth factors improve immediate survival of embryonic dopamine neurons after transplantation into rats. Brain Res. 786:1998;96-103.