BDNF enhances the functional reinnervation of the striatum by grafted fetal dopamine neurons

Experimental Neurology

Volumn 137, Issue 1, 1996, Pages 105-118

  Yurek, David M ^a   Lu, William ^a   Hipkens, Susan ^a   Wiegand, Stanley J ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; BRAIN DERIVED NEUROTROPHIC FACTOR; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CIRCLING BEHAVIOR; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; FETUS; IMMUNOCYTOCHEMISTRY; LOCOMOTION; MALE; NERVE GRAFT; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SUBSTANTIA NIGRA;

EID: 0030053470     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1996.0011     Document Type: Article

References (66)

1. ACHESON, A., J. C. CONOVER, J. P. FANDL, T. M. DECHIARA, M. RUSSELL, A. THADANI, S. P. SQUINTO, G. D. YANCOPOULOS, AND R. M. LINDSAY. 1995. A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374: 450-453.
2. ALEXI, T., AND F. HEFTI. 1993. Trophic actions of transforming growth factor alpha on mesencephalic dopaminergic neurons developing in culture. Neuroscience 55: 903-918.
3. ALTAR, C. A., C. B. BOYLAN, S. HERSHENSON, J. MILLER, S. J. WIEGAND, R. M. LINDSAY, AND C. HYMAN. 1992. Brain-derived neurotrophic factor augments rotational behavior and nigrostriatal dopamine turnover in vivo. Proc. Natl. Acad. Sci. USA 89: 11347-11351.
4. ANDERSON, K. D., R. F. ALDERSON, C. A. ALTAR, P. DISTEFANO, T. L. CORCORAN, R. M. LINDSAY, AND S. J. WIEGAND. 1995. The differential distribution of exogenous BDNF and NGF in the brain corresponds to the distributions of high-affinity and low-affinity neurotrophin receptors. J. Comp. Neurol. 357: 296-317.
5. BECK, K. D., B. KNÜSEL, AND F. HEFTI. 1993. The nature of the trophic action of brain-derived neurotrophic factor, des(1-3)-insulin-like growth factor-1, and basic fibroblast growth factor on mesencephalic dopaminergic neurons developing in culture. Neuroscience 52: 855-866.
6. BJÖRKLUND, A., U. STENEVI, R. H. SCHMIDT, S. B. DUNNETT, AND F. H. GAGE. 1983. Intracerebral grafting of neuronal cell suspensions. II. Survival and growth of nigral cell suspensions implanted in different brain sites. Acta Physiol. Scand. 522: 9-16.
7. BOLAM, J. P., T. F. FREUND, A. BJÖRKLUND, S. B. DUNNETT, AND A. D. SMITH. 1987. Synaptic input and local output of dopaminergic neurons in grafts that functionally reinnervate the host neostriatum. Exp. Brain Res. 68: 131-146.
8. BRUNDIN, P., R. E. STRECKER, O. LINDVALL, O. ISACSON, O. G. NILSSON, G. BARDIN, A. PROCHIANTZ, C. FORNI, A. NIEOULLON, H. WIDNER, F. H. GAGE, AND A. BJÖRKLUND. 1987. Intracerebral grafting of dopamine neurons. Ann. N. Y. Acad. Sci. 495: 473-496.
9. CASPER, D., C. MYTILINEOU, AND M. BLUM. 1991. EGF enhances the survival of dopamine neurons in rat embryonic mesencephalon primary cell culture. J. Neurosci. Res. 30: 372-381.
10. COYLE, J. T., AND P. CAMPOCHIARO. 1976. Ontogenesis of dopaminergic-cholinergic interactions in the rat striatum: A Neurochemical study. J. Neurochem. 27: 673-678.
11. ENGELE, J., D. SCHUBERT, AND M. C. BOHN. 1991. Conditioned media derived from glial cell lines promote survival and differentiation of dopaminergic neurons in vitro: Role of mesencephalic glia. J. Neurosci. Res. 30: 359-371.
12. ERNFORS, P., C. WETMORE, L. OLSON, AND H. PERSSON. 1990. Identification of cells in rat brain and peripheral tissue expressing messenger RNA for members of the nerve growth factor family. Neuron 5: 511-526.
13. FREED, C. R., R. E. BREEZE, N. L. ROSENBERG, S. A. SCHNECK, E. KRIEK, J.-X. QI, T. LONE, Y. B. ZHANG, J. A. SNYDER, T. H. WELLS, L. O. RAMIG, L. THOMPSON, J. C. MAZZIOTTA, S. C. HUANG, S. T. GRAFTON, D. BROOKS, G. SAWLE, G. SCHROTER, AND A. A. ANSARI. 1992. Survival of implanted fetal dopamine cells and neurological improvement 12 to 46 months after transplantation for Parkinson's disease. N. Engl J. Med. 327: 1549-1555.
14. FREED, C. R., R. E. BREEZE, N. L. ROSENBERG, S. A. SCHNECK, T. H. WELLS, J. N. BARRETT, S. T. GRAFTON, S. C. HUANG, D. EIDELBERG, AND D. A. ROTTENBERG. 1990. Transplantation of human fetal dopamine cells for Parkinson's disease. Arch. Neurol. 47: 505-512.
15. FREED, W. J. 1990. Fetal brain grafts and Parkinson's disease. Science 250: 1434.
16. FREUND, T. F., J. P. BOLAM, A. BJÖRKLUND, U. STENEVI, S. B. DUNNETT, J. F. POWELL, AND A. D. SMITH. 1985. Efferent synaptic connections or grafted dopaminergic neurons innervating the host neostriatum: A tyrosine hydroxylase immunocytochemical study. J. Neurosci. 5: 603-616.
17. FRIEDMAN, W. J., L. OLSON, AND J. PERSSON. 1991. Cells that express brain-derived neurotrophic factor mRNA in the developing postnatal rat brain. Eur. J. Neurosci. 3: 688-697.
18. GALL, C. M., S. J. GOLD, P. J. ISACKSON, AND K. B. SEROOGY. 1992. Brain-derived neurotrophic factor and neurotrophin-3 mRNAs are expressed in ventral midbrain regions containing dopaminergic neurons. Mol. Cell. Neurosci. 3: 56-63.
19. GIACOBINI, M. M. J., S. ALSTRÖM, K. FUNA, AND L. OLSON. 1993. Differential effects of platelet-derived growth factor isoforms on dopamine neurons in vivo. I. Supports cell survival. II. Enhances fiber formation. Neuroscience 57: 923-929.
20. GIACOBINI, M. M. J., I. STRÖMBERG, S. ALSTRÖM, Y. H. CAO, AND L. OLSON. 1993. Fibroblast growth factors enhance dopamine fiber formation from nigral grafts. Dev. Brain Res. 75: 65-73.
21. HATTORI, T., AND P. L. MCGEER. 1973. Synaptogenesis in the corpus striatum of infant rat. Exp. Neurol. 38: 70-79.
22. HSU, S.-M., AND L. RAINE. 1981. Protein A, avidin and biotin in immunocytochemistry. J. Histochem. Cytochem. 29: 1349-1353.
23. HYMAN, C., M. HOFER, Y.-A. BARDE, M. JUHASZ, G. D. YANCOPOULOS, S. P. SQUINTO, AND R. M. LINDSAY. 1991. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350: 230-232.
24. HYMAN, C., M. JUHASZ, C. JACKSON, P. WRIGHT, N. Y. IP, AND R. M. LINDSAY. 1994. Overlapping and distinct actions of the neurotrophins BDNF, NT-3, and NT-4/5 on cultured dopaminergic and gabaergic neurons of the ventral mesencephalon. J. Neurosci. 14: 335-347.
25. JAEGER, C. B. 1985. Cytoarchitecture of substantia nigra grafts: Alight and electron microscopic study of immunocytochemically identified dopaminergic neurons and fibrous astrocytes. J. Comp. Neurol. 231: 121-135.
26. JANEC, E., AND R. E. BURKE. 1993. Naturally occurring cell death during postnatal development of the substantia nigra pars compacta of rat. Mol. Cell. Neurosci. 4: 30-35.
27. KNÜSEL, B., J. WINSLOW, A. ROSENTHAL, L. BURTON, D. SEID, K. NIKOLICS, AND F. HEFTI. 1991. Promotion of central cholinergic and dopaminergic neuron differentiation by brain-derived neurotrophic factor but not neurotrophin-3. Proc. Natl. Acad. Sci. USA 88: 961-965.
28. KORDOWER, J. H., D. L. FELTON, AND D. M. GASH. 1992. Neural grafting for Parkinson's disease. Pages 175-224 in C. W. Olanow and A. N. Lieberman, Eds., The Scientific Basis for the Treatment of Parkinson's Disease. Parthenon, New York.
29. KORDOWER, J. H., T. B. FREEMAN, B. J. SNOW, F. J. G. VINGER-HOETS, E. J. MUFSON, P. R. SANBERG, R. A. HAUSER, D. A. SMITH, M. NAUERT, D. P. PERL, AND C. W. OLANOW. 1995. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. N. Engl. J. Med. 332: 1118-1124.
30. KORDOWER, J. H., E. J. MUFSON, A.-C. GRANHOLM, B. J. HOFFER, AND P. M. FRIDEN. 1993. Delivery of trophic factors to the primate brain. Exp. Neurol. 124: 21-30.
31. LAPCHAK, P. A., AND F. HEFTI. 1992. BDNF and NGF treatment in lesioned rats: Effects on cholinergic function and weight gain. NeuroReport 3: 405-408.
32. LIN, L. H., D. H. DOHERTY, J. D. LILE, S. BEKTESH, AND F. COLLINS. 1993. GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260: 1130-1132.
33. LINDSAY, R. M., C. A. ALTAR, J. M. CEDARBAUM, C. HYMAN, AND S. J. WIEGAND. 1993. The therapeutic potential of neurotrophic factors in the treatment of Parkinson's disease. Exp. Neurol. 124: 103-118.
34. LINDSAY, R. M., S. J. WIEGAND, C. A. ALTAR, AND P. S. DISTEFANO. 1994. Neurotrophic factors: From molecule to man. Trends Neurosci. 17: 182-190.
35. LINDVALL, O. 1989. Transplantation into the human brain: Present status and future possibilities. J. Neurol. Neurosurg. Psychiat. (Suppl.): 39-54.
36. LINDVALL, O., AND A. BJÖRKLUND. 1989. Transplantation strategies in the treatment of Parkinson's disease: Experimental basis and clinical trials. Acta Neurol. Scand. 126: 197-210.
37. LINDVALL, O., P. BRUNDIN, AND H. WIDNER, 1990. Grafts of fetal dopamine neurons survive and improve motor function in Parkinson's disease. Science 247: 575-577.
38. LINDVALL, O., S. RECHNCRONA, P. BRUNDIN, B. GUSTAVII, B. ASTEDT, H. WIDNER, T. LINDHOLM, A. BJÖRKLUND, K. L. LEENDERS, J. C. ROTHWELL, R. FRACKOWIAK, C. D. MARSDEN, B. JOHNELS, G. STEG, R. FREEDMAN, B. J. HOFFER, A. SEIGER, M. BYGDEMAN, I. STRÖMBERG, AND L. OLSON. 1989. Human fetal dopamine neurons grafted into the striatum in two patients with severe Parkinson's disease. Arch. Neurol. 46: 615-631.
39. LINDVALL, O., H. WIDNER, S. REHNCRONA, P. BRUNDIN, P. ODIN, B. GUSTAVII, R. FRACKOWIAK, K. L. LEENDERS, G. SAWLE, J. C. ROTHWELL, A. BJÖRKLUND, AND C. D. MARSDEN. 1992. Transplantation of fetal dopamine neurons in Parkinson's disease: One-year clinical and neurophysiological observations in two patients with putaminal implants. Ann. Neurol. 31: 155-165.
40. LOIZOU, L. A. 1972. The postnatal ontogeny of monoamine-containing neurones in the central nervous system of the albino rat. Brain Res. 40: 395-418.
41. LU, W., D. M. YUREK, S. B. HIPKENS, AND S. J. WIEGAND. 1994. Effect of BDNF on fetal mesencephalic grafts: A microdialysis study. 5th Int. Symp. Neural Transplantation. [Abstract]
42. MADRAZO, I., R. FRANCO-BOURLAND, F. OSTROSKY-SOLIS, M. AGUILERA, C. CUEVAS, C. ZAMORANO, A. MORELOS, E. MAGALLON, AND G. GUIZAR-SAHAGUN. 1990. Fetal homotransplants (ventral mesencephalon and adrenal tissue) to the striatum of parkinsonian subjects. Arch. Neurol 47: 1281-1285.
43. MAHALIK, T. J., T. E. FINGER, I. STROMBERG, AND L. OLSON. 1985. Substantia nigra transplants into denervated striatum of the rat: Ultrastructure of graft and host interconnections. J. Comp. Neurol. 240: 60-70.
44. MAISONPIERRE, P. C., L. BELLUSCIO, B. FRIEDMAN, F. ALDERSON, S. J. WIEGAND, M. E. FURTH, R. M. LINDSAY, AND G. D. YANCOPOULOS. 1990. NT-3, BDNF, and NGF in the developing rat nervous system: Parallel as well as reciprocal patterns of expression. Neuron 5: 501-509.
45. MANDEL, R. J., P. BRUNDIN, AND A. BJÖRKLUND. 1990. 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: 888-894.
46. MAYER, E., J. W. FAWCETT, AND S. B. DUNNETT. 1993. Basic fibroblast growth factor promotes the survival of embryonic ventral mesencephalic dopaminergic neurons. II. Effects on nigral transplants in vivo. Neuroscience 56: 389-398.
47. MYTILINEOU, C., T. H. PARK, AND J. SHEN. 1992. Epidermal growth factor induced survival and proliferation of neuronal precursor cells from embryonic rat mesencephalon. Neurosci. Lett. 135: 62-66.
48. OLSON, L., Å. SEIGER, AND K. FUXE. 1972. Heterogeneity of striatal and limbic dopamine innervation: Highly fluorescent islands in developing and adult rats. Brain Res. 44: 283-288.
49. OTTO, D., AND K. UNSICKER 1990. Basic FGF reverses chemical and morphological deficits in the nigrostriatal system of MPTP-treated mice. J. Neurosci. 10: 1912-1921.
50. PEZZOLI, G., A. ZECCHINELLI, S. RICCIARDI, R. E. BURKE, S. FAHN, G. SCARLATO, AND A. CARENZI. 1991. Intraventricular infusion of epidermal growth factor restores dopaminergic pathway in hemiparkinsonian rats. Movement Disorders 6: 281-287.
51. PHILLIPS, H., J. M. HAINS, M. ARMANINI, G. R. LARAMEE, S. A. JOHNSON, AND J. W. WINSLOW. 1991. BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 7: 695-702.
52. SAUER, H., K. CAMPBELL, S. J. WIEGAND, R. M. LINDSAY, AND A. BJÖRKLUND. 1994. Brain-derived neurotrophic factor enhances striatal neuropeptide expression in both the intact and the dopamine-depleted rat striatum. NeuroReport 5: 609-612.
53. SAUER, H., W. FISCHER, G. NIKKHAH, S. J. WIEGAND, P. BRUNDIN, R. M. LINDSAY, AND A. BJÖRKLUND. 1993. Brain-derived neurotrophic factor enhances function rather than survival of intrastriatal dopamine cell-rich grafts. Brain Res. 626: 37-44.
54. SEROOGY, K. B., AND C. M. GALL. 1993. Expression of neurotrophins by midbrain dopaminergic neurons. Exp. Neurol. 124: 119-128.
55. SLADEK, J. R., JR., T. J. COLLIER, S. N. HABER, R. H. ROTH, AND D. E. REDMOND. 1986. Survival and growth of fetal catecholamine neurons transplanted into primate brain. Brain Res. Bull. 17: 809-818.
56. SNIDER, W. D., AND E. M. JOHNSON. 1989. Neurotrophic molecules. Ann. Neurol. 26: 489-506.
57. SPENCER, D. D., R. J. ROBBINS, F. NAFTOLIN, K. L. MAREK, T. VOLLMER, C. LERANTH, R. H. ROTH, L. H. PRICE, A. GJEDDE, B. S. BUNNEY, K. J. SASS, J. D. ELSWORTH, E. L. KIER, R. MAKUCH, P. B. HOFFER, AND D. E. REDMOND. 1992. Unilateral transplantation of human fetal mesencephalic tissue into the caudate nucleus of patients with Parkinson's disease. N. Engl. J. Med. 327: 1541-1548.
58. SPENGER, C. 1995. BDNF and cultured human neurons. Exp. Neurol., 133: 50-63.
59. SPINA, M. B., S. P. SQUINTO, J. MILLER, R. M. LINDSAY, AND C. HYMAN. 1992. Brain-derived neurotrophic factor protects dopamine neurons against 6-hydroxydopamine and n-methyl-4-phenylpyridinium ion toxicity: Involvement of the glutathione system. J. Neurochem. 59: 99-106.
60. STROMBERG, I., L. BJORKLUND, M. JOHANSSON, A. TOMAC, F. COLLINS, L. OLSON, B. HOFFER, AND C. HUMPEL. 1993. Glial cell line-derived neurotrophic factor is expressed in the developing but not adult striatum and stimulates developing dopamine neurons in vivo. Exp. Neurol. 124: 401-412.
61. TAKAYAMA, H., J. RAY, H. K. RAYMON, A. BAIRD, J. HOGG, L. J. FISHER, AND F. H. GAGE. 1995. Basic fibroblast growth factor increases dopaminergic graft survival and function in a rat model of Parkinson's disease. Nat. Med. 1: 53-58.
62. 3H]dopamine uptake. Brain Res. 46: 251-285.
63. THOENEN, H. 1991. The changing scene of neurotrophic factors. Trends Neurosci. 14: 165-170.
64. WHITMAN, M., AND D. A. MELTON. 1989. Growth factors in early embryogenesis. Annu. Rev. Cell Biol. 5: 93-117.
65. WIDNER, H., J. TETRUD, S. REHNCRONA, B. SNOW, P. BRUNDIN, B. GUSTAVII, A. BJÖRKLUND, O. LINDVALL, AND J. W. LANGSTON. 1992. Bilateral fetal mesencephalic grafting in two patients with parkinsonism induced by 1-methyl-4-phenyl-1,2,3,6-tetrahy-dropyridine (MPTP). N. Engl. J. Med. 327: 1556.
66. YUREK, D. M., AND J. R. SLADEK, JR. 1990. Dopamine cell replacement: Parkinson's disease. Annu. Rev. Neurosci. 13: 415-440.