Cytoprotective effects of growth factors: BDNF more potent than GDNF in an organotypic culture model of Parkinson's disease

Brain Research

Volumn 1378, Issue , 2011, Pages 105-118

  Stahl, K ^a   Mylonakou, M N ^a   Skare, O ^b,c   Amiry Moghaddam, M ^a   Torp, R ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^c UNIVERSITY OF BERGEN   (Norway)

Author keywords

BDNF; Cytoprotection; Dopaminergic cell; GDNF; Organotypic culture; Parkinson's disease

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; OXIDOPAMINE; TYROSINE 3 MONOOXYGENASE; VESICULAR MONOAMINE TRANSPORTER 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG POTENCY; FEMALE; IMMUNOFLUORESCENCE TEST; MALE; MESENCEPHALON; NERVE REGENERATION; NERVE SPROUTING; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REGENERATIVE ABILITY; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM;

ADRENERGIC AGENTS; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DOPAMINE; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; MICROSCOPY, CONFOCAL; NEURONS; NEUROPROTECTIVE AGENTS; ORGAN CULTURE TECHNIQUES; OXIDOPAMINE; PARKINSON DISEASE; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

RATTUS;

EID: 79951947978     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.12.090     Document Type: Article

References (98)

1. af Bjerkén, S., Boger, H.A., Nelson, M., Hoffer, B.J., Granholm, A.C., Stromberg, I., 2007. Effects of glial cell line-derived neurotrophic factor deletion on ventral mesencephalic organotypic tissue cultures. Brain Res. 1133, 10-19.
2. Akerud, P., Alberch, J., Eketjall, S., Wagner, J., Arenas, E., 1999. Differential effects of glial cell line-derived neurotrophic factor and neurturin on developing and adult substantia nigra dopaminergic neurons. J. Neurochem. 73, 70-78. (Pubitemid 29289112)
3. Altar, C.A., DiStefano, P.S., 1998. Neurotrophin trafficking by anterograde transport. Trends Neurosci. 21, 433-437. (Pubitemid 28449073)
4. Atwal, J.K., Massie, B., Miller, F.D., Kaplan, D.R., 2000. The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase. Neuron 27, 265-277.
5. Barroso-Chinea, P., Cruz-Muros, I., Aymerich, M.S., Rodriguez-Diaz, M., Afonso-Oramas, D., Lanciego, J.L., Gonzalez-Hernandez, T., 2005. Striatal expression of GDNF and differential vulnerability of midbrain dopaminergic cells. Eur. J. Neurosci. 21, 1815-1827.
6. Bibel, M., Hoppe, E., Barde, Y.A., 1999. Biochemical and functional interactions between the neurotrophin receptors trk and p75NTR. EMBO J. 18, 616-622. (Pubitemid 29057246)
7. Bilang-Bleuel, A., Revah, F., Colin, P., Locquet, I., Robert, J.J., Mallet, J., Horellou, P., 1997. Intrastriatal injection of an adenoviral vector expressing glial-cell-line-derived neurotrophic factor prevents dopaminergic neuron degeneration and behavioral impairment in a rat model of Parkinson disease. Proc. Natl Acad. Sci. USA 94, 8818-8823.
8. Binder, D.K., Croll, S.D., Gall, C.M., Scharfman, H.E., 2001. BDNF and epilepsy: too much of a good thing? Trends Neurosci. 24, 47-53.
9. Bishop, A.L., Hall, A., 2000. Rho GTPases and their effector proteins. Biochem. J. 348 (Pt 2), 241-255. (Pubitemid 30345195)
10. Blesch, A., Grill, R.J., Tuszynski, M.H., 1998. Neurotrophin gene therapy in CNS models of trauma and degeneration. Prog. Brain Res. 117, 473-484.
11. Brunet, A., Datta, S.R., Greenberg, M.E., 2001. Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11, 297-305.
12. Burke, R.E., Antonelli, M., Sulzer, D., 1998. Glial cell line-derived neurotrophic growth factor inhibits apoptotic death of postnatal substantia nigra dopamine neurons in primary culture. J. Neurochem. 71, 517-525. (Pubitemid 28480398)
13. Carmignoto, G., Pizzorusso, T., Tia, S., Vicini, S., 1997. Brain-derived neurotrophic factor and nerve growth factor potentiate excitatory synaptic transmission in the rat visual cortex. J. Physiol. 498 (Pt 1), 153-164. (Pubitemid 27056886)
14. Carter, B.D., Zirrgiebel, U., Barde, Y.A., 1995. Differential regulation of p21ras activation in neurons by nerve growth factor and brain-derived neurotrophic factor. J. Biol. Chem. 270, 21751-21757.
15. Cohen-Cory, S., 1999. BDNF modulates, but does not mediate, activity-dependent branching and remodeling of optic axon arbors in vivo. J. Neurosci. 19, 9996-10003. (Pubitemid 30226671)
16. Cohen-Cory, S., Fraser, S.E., 1995. Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378, 192-196.
17. Connor, B., Dragunow, M., 1998. The role of neuronal growth factors in neurodegenerative disorders of the human brain. Brain Res. Brain Res. Rev. 27, 1-39.
18. Croll, S.D., Suri, C., Compton, D.L., Simmons, M.V., Yancopoulos, G.D., Lindsay, R.M., Wiegand, S.J., Rudge, J.S., Scharfman, H.E., 1999. Brain-derived neurotrophic factor transgenic mice exhibit passive avoidance deficits, increased seizure severity and in vitro hyperexcitability in the hippocampus and entorhinal cortex. Neuroscience 93, 1491-1506. (Pubitemid 29397578)
19. Datta, S.R., Brunet, A., Greenberg, M.E., 1999. Cellular survival: a play in three Akts. Genes Dev. 13, 2905-2927.
20. Ebadi, M., Bashir, R.M., Heidrick, M.L., Hamada, F.M., Refaey, H.E., Hamed, A., Helal, G., Baxi, M.D., Cerutis, D.R., Lassi, N.K., 1997. Neurotrophins and their receptors in nerve injury and repair. Neurochem. Int. 30, 347-374.
21. Erickson, J.T., Brosenitsch, T.A., Katz, D.M., 2001. Brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor are required simultaneously for survival of dopaminergic primary sensory neurons in vivo. J. Neurosci. 21, 581-589. (Pubitemid 32107447)
22. Feng, L., Wang, C.Y., Jiang, H., Oho, C., Dugich-Djordjevic, M., Mei, L., Lu, B., 1999. Differential signaling of glial cell line-derived neurothrophic factor and brain-derived neurotrophic factor in cultured ventral mesencephalic neurons. Neuroscience 93, 265-273. (Pubitemid 29290706)
23. Frank, L., Ventimiglia, R., Anderson, K., Lindsay, R.M., Rudge, J.S., 1996. BDNF down-regulates neurotrophin responsiveness, TrkB protein and TrkB mRNA levels in cultured rat hippocampal neurons. Eur. J. Neurosci. 8, 1220-1230.
24. Frim, D.M., Uhler, T.A., Galpern, W.R., Beal, M.F., Breakefield, X.O., Isacson, O., 1994. Implanted fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevent 1-methyl-4-phenylpyridinium toxicity to dopaminergic neurons in the rat. Proc. Natl. Acad. Sci. USA 91, 5104-5108.
25. Galpern, W.R., Frim, D.M., Tatter, S.B., Altar, C.A., Beal, M.F., Isacson, O., 1996. Cell-mediated delivery of brain-derived neurotrophic factor enhances dopamine levels in an MPP+ rat model of substantia nigra degeneration. Cell Transplant. 5, 225-232. (Pubitemid 26096182)
26. Gash, D.M., Zhang, Z., Cass, W.A., Ovadia, A., Simmerman, L., Martin, D., Russell, D., Collins, F., Hoffer, B.J., Gerhardt, G.A., 1995. Morphological and functional effects of intranigrally administered GDNF in normal rhesus monkeys. J. Comp. Neurol. 363, 345-358.
27. Gash, D.M., Zhang, Z., Ovadia, A., Cass, W.A., Yi, A., Simmerman, L., Russell, D., Martin, D., Lapchak, P.A., Collins, F., Hoffer, B.J., Gerhardt, G.A., 1996. Functional recovery in parkinsonian monkeys treated with GDNF. Nature 380, 252-255. (Pubitemid 26090648)
28. Georgievska, B., Carlsson, T., Lacar, B., Winkler, C., Kirik, D., 2004. Dissociation between short-term increased graft survival and long-term functional improvements in Parkinsonian rats overexpressing glial cell line-derived neurotrophic factor. Eur. J. Neurosci. 20, 3121-3130.
29. Gerfen, C.R., Herkenham, M., Thibault, J., 1987. The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J. Neurosci. 7, 3915-3934.
30. Gill, S.S., Patel, N.K., Hotton, G.R., O'Sullivan, K., McCarter, R., Bunnage, M., Brooks, D.J., Svendsen, C.N., Heywood, P., 2003. Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat. Med. 9, 589-595.
31. Goldberg, J.L., Espinosa, J.S., Xu, Y., Davidson, N., Kovacs, G.T., Barres, B.A., 2002. Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 33, 689-702. (Pubitemid 34219241)
32. Grondin, R., Cass, W.A., Zhang, Z., Stanford, J.A., Gash, D.M., Gerhardt, G.A., 2003. Glial cell line-derived neurotrophic factor increases stimulus-evoked dopamine release and motor speed in aged rhesus monkeys. J. Neurosci. 23, 1974-1980. (Pubitemid 36314753)
33. Grondin, R., Gash, D.M., 1998. Glial cell line-derived neurotrophic factor (GDNF): a drug candidate for the treatment of Parkinson's disease. J. Neurol. 245, 35-42.
34. Grondin, R., Zhang, Z., Yi, A., Cass, W.A., Maswood, N., Andersen, A.H., Elsberry, D.D., Klein, M.C., Gerhardt, G.A., Gash, D.M., 2002. Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain 125, 2191-2201.
35. Hacein-Bey-Abina, S., Garrigue, A., Wang, G.P., Soulier, J., Lim, A., Morillon, E., Clappier, E., Caccavelli, L., Delabesse, E., Beldjord, K., Asnafi, V., MacIntyre, E., Dal, C.L., Radford, I., Brousse, N., Sigaux, F., Moshous, D., Hauer, J., Borkhardt, A., Belohradsky, B. H., Wintergerst, U., Velez, M.C., Leiva, L., Sorensen, R., Wulffraat, N., Blanche, S., Bushman, F.D., Fischer, A., Cavazzana-Calvo, M., 2008. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 118, 3132-3142.
36. Harada, A., Teng, J., Takei, Y., Oguchi, K., Hirokawa, N., 2002. MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J. Cell Biol. 158, 541-549. (Pubitemid 34851712)
37. Hetman, M., Kanning, K., Cavanaugh, J.E., Xia, Z., 1999. Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase. J. Biol. Chem. 274, 22569-22580.
38. Horch, H.W., Kruttgen, A., Portbury, S.D., Katz, L.C., 1999. Destabilization of cortical dendrites and spines by BDNF. Neuron 23, 353-364. (Pubitemid 29315729)
39. Huang, E.J., Reichardt, L.F., 2001. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
40. Hyman, C., Hofer, M., Barde, Y.A., Juhasz, M., Yancopoulos, G.D., Squinto, S.P., Lindsay, R.M., 1991. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350, 230-232. (Pubitemid 21912205)
41. Jakobsen, B., Gramsbergen, J.B., Moller, D.A., Rosenblad, C., Zimmer, J., 2005. Characterization of organotypic ventral mesencephalic cultures from embryonic mice and protection against MPP toxicity by GDNF. Eur. J. Neurosci. 21, 2939-2948.
42. Kaplan, D.R., Miller, F.D., 2000. Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-391.
43. Kearns, C.M., Gash, D.M., 1995. GDNF protects nigral dopamine neurons against 6-hydroxydopamine in vivo. Brain Res. 672, 104-111.
44. Klein, R.L., Lewis, M.H., Muzyczka, N., Meyer, E.M., 1999. Prevention of 6-hydroxydopamine-induced rotational behavior by BDNF somatic gene transfer. Brain Res. 847, 314-320.
45. Knusel, B., Winslow, J.W., Rosenthal, A., Burton, L.E., Seid, D.P., Nikolics, K., Hefti, F., 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.
46. Kordower, J.H., Emborg, M.E., Bloch, J., Ma, S.Y., Chu, Y., Leventhal, L., McBride, J., Chen, E.Y., Palfi, S., Roitberg, B.Z., Brown, W.D., Holden, J.E., Pyzalski, R., Taylor, M.D., Carvey, P., Ling, Z., Trono, D., Hantraye, P., Deglon, N., Aebischer, P., 2000. Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson's disease. Science 290, 767-773.
47. Kordower, J.H., Palfi, S., Chen, E.Y., Ma, S.Y., Sendera, T., Cochran, E.J., Cochran, E.J., Mufson, E.J., Penn, R., Goetz, C.G., Comella, C.D., 1999. Clinicopathological findings following intraventricular glial-derived neurotrophic factor treatment in a patient with Parkinson's disease. Ann. Neurol. 46, 419-424.
48. Lang, A.E., Gill, S., Patel, N.K., Lozano, A., Nutt, J.G., Penn, R., Brooks, D.J., Hotton, G., Moro, E., Heywood, P., Brodsky, M.A., Burchiel, K., Kelly, P., Dalvi, A., Scott, B., Stacy, M., Turner, D., Wooten, V.G., Elias, W.J., Laws, E.R., Dhawan, V., Stoessl, A.J., Matcham, J., Coffey, R.J., Traub, M., 2006. Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease. Ann. Neurol. 59, 459-466.
49. Levivier, M., Przedborski, S., Bencsics, C., Kang, U.J., 1995. Intrastriatal implantation of fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevents degeneration of dopaminergic neurons in a rat model of Parkinson's disease. J. Neurosci. 15, 7810-7820. (Pubitemid 26006890)
50. Lin, L.F., Doherty, D.H., Lile, J.D., Bektesh, S., Collins, F., 1993. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260, 1130-1132. (Pubitemid 23186789)
51. Lindholm, P., Voutilainen, M.H., Lauren, J., Peranen, J., Leppanen, V.M., Andressoo, J.O., Lindahl, M., Janhunen, S., Kalkkinen, N., Timmusk, T., Tuominen, R.K., Saarma, M., 2007. Novel neurotrophic factor CDNF protects and rescues midbrain dopamine neurons in vivo. Nature 448, 73-77. (Pubitemid 47037006)
52. Lindvall, O., Kokaia, Z., Bengzon, J., Elmer, E., Kokaia, M., 1994. Neurotrophins and brain insults. Trends Neurosci. 17, 490-496. (Pubitemid 24321951)
53. Lindvall, O., Wahlberg, L.U., 2008. Encapsulated cell biodelivery of GDNF: a novel clinical strategy for neuroprotection and neuroregeneration in Parkinson's disease? Exp. Neurol. 209, 82-88.
54. Liu, B.P., Burridge, K., 2000. Vav2 activates Rac1, Cdc42, and RhoA downstream from growth factor receptors but not beta1 integrins. Mol. Cell. Biol. 20, 7160-7169.
55. Lom, B., Cohen-Cory, S., 1999. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J. Neurosci. 19, 9928-9938. (Pubitemid 30226665)
56. Love, S., Plaha, P., Patel, N.K., Hotton, G.R., Brooks, D.J., Gill, S.S., 2005. Glial cell line-derived neurotrophic factor induces neuronal sprouting in human brain. Nat. Med. 11, 703-704.
57. Marco, S., Saura, J., Perez-Navarro, E., Jose, M.M., Tolosa, E., Alberch, J., 2002. Regulation of c-Ret, GFRalpha1, and GFRalpha2 in the substantia nigra pars compacta in a rat model of Parkinson's disease. J. Neurobiol. 52, 343-351. (Pubitemid 34925390)
58. Martinez, A., Alcantara, S., Borrell, V., Del Rio, J.A., Blasi, J., Otal, R., Campos, N., Boronat, A., Barbacid, M., Silos-Santiago, I., Soriano, E., 1998. TrkB and TrkC signaling are required for maturation and synaptogenesis of hippocampal connections. J. Neurosci. 18, 7336-7350. (Pubitemid 28425818)
59. McAllister, A.K., 2000. Cellular and molecular mechanisms of dendrite growth. Cereb. Cortex 10, 963-973.
60. McAllister, A.K., Katz, L.C., Lo, D.C., 1996. Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17, 1057-1064. (Pubitemid 27021093)
61. McAllister, A.K., Katz, L.C., Lo, D.C., 1997. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 18, 767-778. (Pubitemid 27232787)
62. McAllister, A.K., Katz, L.C., Lo, D.C., 1999. Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci. 22, 295-318.
63. McAllister, A.K., Lo, D.C., Katz, L.C., 1995. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15, 791-803.
64. Meyer, M., Zimmer, J., Seiler, R.W., Widmer, H.R., 1999. 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, 25-36. (Pubitemid 29408769)
65. Miller, F.D., Kaplan, D.R., 2003. Signaling mechanisms underlying dendrite formation. Curr. Opin. Neurobiol. 13, 391-398.
66. Mogi, M., Togari, A., Kondo, T., Mizuno, Y., Komure, O., Kuno, S., Ichinose, H., Nagatsu, T., 1999. Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson's disease. Neurosci. Lett. 270, 45-48.
67. Numan, S., Seroogy, K.B., 1997. Increased expression of trkB mRNA in rat caudate-putamen following 6-OHDA lesions of the nigrostriatal pathway. Eur. J. Neurosci. 9, 489-495.
68. Nutt, J.G., Burchiel, K.J., Comella, C.L., Jankovic, J., Lang, A.E., Laws Jr., E.R., Lozano, A.M., Penn, R.D., Simpson Jr., R.K., Stacy, M., Wooten, G.F., 2003. Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology 60, 69-73. (Pubitemid 36070646)
69. Parain, K., Murer, M.G., Yan, Q., Faucheux, B., Agid, Y., Hirsch, E., Raisman-Vozari, R., 1999a. Reduced expression of brain-derived neurotrophic factor protein in Parkinson's disease substantia nigra. NeuroReport 10, 557-561. (Pubitemid 29333282)
70. Parain, K., Murer, M.G., Yan, Q., Faucheux, B., Agid, Y., Hirsch, E., Raisman-Vozari, R., 1999b. Reduced expression of brain-derived neurotrophic factor protein in Parkinson's disease substantia nigra. NeuroReport 10, 557-561. (Pubitemid 29333282)
71. Pascual, A., Hidalgo-Figueroa, M., Piruat, J.I., Pintado, C.O., Gomez-Diaz, R., Lopez-Barneo, J., 2008. Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat. Neurosci. 11, 755-761.
72. Patel, N.K., Bunnage, M., Plaha, P., Svendsen, C.N., Heywood, P., Gill, S.S., 2005. Intraputamenal infusion of glial cell line-derived neurotrophic factor in PD: a two-year outcome study. Ann. Neurol. 57, 298-302.
73. Petrova, P., Raibekas, A., Pevsner, J., Vigo, N., Anafi, M., Moore, M.K., Peaire, A.E., Shridhar, V., Smith, D.I., Kelly, J., Durocher, Y., Commissiong, J.W., 2003. MANF: a new mesencephalic, astrocyte-derived neurotrophic factor with selectivity for dopaminergic neurons. J. Mol. Neurosci. 20, 173-188.
74. Reeben, M., Laurikainen, A., Hiltunen, J.O., Castren, E., Saarma, M., 1998. The messenger RNAs for both glial cell line-derived neurotrophic factor receptors, c-ret and GDNFRalpha, are induced in the rat brain in response to kainate-induced excitation. Neuroscience 83, 151-159. (Pubitemid 28068045)
75. Sariola, H., Saarma, M., 2003. Novel functions and signalling pathways for GDNF. J. Cell Sci. 116, 3855-3862. (Pubitemid 37279301)
76. Sautter, J., Meyer, M., Spenger, C., Seiler, R.W., Widmer, H.R., 1998. Effects of combined BDNF and GDNF treatment on cultured dopaminergic midbrain neurons. NeuroReport 9, 1093-1096. (Pubitemid 28266629)
77. Shingo, T., Date, I., Yoshida, H., Ohmoto, T., 2002. Neuroprotective and restorative effects of intrastriatal grafting of encapsulated GDNF-producing cells in a rat model of Parkinson's disease. J. Neurosci. Res. 69, 946-954.
78. Shults, C.W., Kimber, T., Altar, C.A., 1995. BDNF attenuates the effects of intrastriatal injection of 6-hydroxydopamine. NeuroReport 6, 1109-1112.
79. Siegel, G.J., Chauhan, N.B., 2000. Neurotrophic factors in Alzheimer's and Parkinson's disease brain. Brain Res. Brain Res. Rev. 33, 199-227.
80. Slevin, J.T., Gash, D.M., Smith, C.D., Gerhardt, G.A., Kryscio, R., Chebrolu, H., Walton, A., Wagner, R., Young, A.B., 2007. Unilateral intraputamenal glial cell line-derived neurotrophic factor in patients with Parkinson disease: response to 1 year of treatment and 1 year of withdrawal. J. Neurosurg. 106, 614-620. (Pubitemid 46536457)
81. Sonntag, K.C., Simunovic, F., Sanchez-Pernaute, R., 2009. Stem cells and cell replacement therapy for Parkinson's disease. J. Neural Transm. Suppl. 287-299.
82. Spina, M.B., Squinto, S.P., Miller, J., Lindsay, R.M., Hyman, C., 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.
83. Stahl, K., Skare, O., Torp, R., 2009. Organotypic cultures as a model of Parkinson s disease. A twist to an old model. Sci. World Journal 9, 811-821.
84. Sun, M., Kong, L., Wang, X., Lu, X.G., Gao, Q., Geller, A.I., 2005. Comparison of the capability of GDNF, BDNF, or both, to protect nigrostriatal neurons in a rat model of Parkinson's disease. Brain Res. 1052, 119-129. (Pubitemid 41116769)
85. Takumi, Y., Ramirez-Leon, V., Laake, P., Rinvik, E., Ottersen, O.P., 1999. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat. Neurosci. 2, 618-624.
86. Tolwani, R.J., Buckmaster, P.S., Varma, S., Cosgaya, J.M., Wu, Y., Suri, C., Shooter, E.M., 2002. BDNF overexpression increases dendrite complexity in hippocampal dentate gyrus. Neuroscience 114, 795-805. (Pubitemid 35247664)
87. Tomac, A., Lindqvist, E., Lin, L.F., Ogren, S.O., Young, D., Hoffer, B.J., Olson, L., 1995. Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 373, 335-339.
88. Torp, R., Ottersen, O.P., Cotman, C.W., Head, E., 2003. Identification of neuronal plasma membrane microdomains that colocalize beta-amyloid and presenilin: implications for beta-amyloid precursor protein processing Neuroscience 120, 291-300.
89. Torp, R., Singh, P.B., Sorensen, D.R., Dietrichs, E., Hirschberg, H., 2006. Growth factors as neuroprotective treatment in Parkinson disease? Tidsskr. Nor. Laegeforen. 126, 899-901.
90. Tsukahara, T., Takeda, M., Shimohama, S., Ohara, O., Hashimoto, N., 1995. Effects of brain-derived neurotrophic factor on 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced parkinsonism in monkeys. Neurosurgery 37, 733-739.
91. Tuszynski, M.H., 2003. Gene therapy for neurological disease. Expert Opin. Biol. Ther. 3, 815-828.
92. Vaillant, A.R., Zanassi, P., Walsh, G.S., Aumont, A., Alonso, A., Miller, F.D., 2002. Signaling mechanisms underlying reversible, activity-dependent dendrite formation. Neuron 34, 985-998. (Pubitemid 34722287)
93. Wang, Y., Sheen, V.L., Macklis, J.D., 1998. Cortical interneurons upregulate neurotrophins in vivo in response to targeted apoptotic degeneration of neighboring pyramidal neurons. Exp. Neurol. 154, 389-402.
94. Xu, B., Zang, K., Ruff, N.L., Zhang, Y.A., McConnell, S.K., Stryker, M.P., Reichardt, L.F., 2000. Cortical degeneration in the absence of neurotrophin signaling: dendritic retraction and neuronal loss after removal of the receptor TrkB. Neuron 26, 233-245.
95. Yan, Q., Radeke, M.J., Matheson, C.R., Talvenheimo, J., Welcher, A.A., Feinstein, S.C., 1997. Immunocytochemical localization of TrkB in the central nervous system of the adult rat. J. Comp. Neurol. 378, 135-157.
96. Yasuhara, T., Date, I., 2007. Intracerebral transplantation of genetically engineered cells for Parkinson's disease: toward clinical application. Cell Transplant. 16, 125-132. (Pubitemid 46668788)
97. Yuan, H., Zhang, Z.W., Liang, L.W., Shen, Q., Wang, X.D., Ren, S.M., Ma, H.J., Jiao, S.J., Liu, P., 2010. Treatment strategies for Parkinson's disease. Neurosci. Bull. 26, 66-76.
98. Zurn, A.D., Winkel, L., Menoud, A., Djabali, K., Aebischer, P., 1996. Combined effects of GDNF, BDNF, and CNTF on motoneuron differentiation in vitro. J. Neurosci. Res. 44, 133-141.