Dopaminergic axon guidance: Which makes what?

Frontiers in Cellular Neuroscience

Volumn , Issue JULY 2012, 2012, Pages

  Prestoz, Laetitia ^a   Jaber, Mohamed ^a   Gaillard, Afsaneh ^a  

^a UNIVERSITÉ DE POITIERS   (France)

Author keywords

Axon guidance; Development; Dopamine; Mesotelencephalic pathway; Parkinson's disease; Transplantation

Indexed keywords

CALBINDIN; EPHRIN RECEPTOR A5; FRIZZLED PROTEIN; NETRIN; PLEXIN; PROTEOGLYCAN; ROBO1 PROTEIN; ROBO2 PROTEIN; ROUNDABOUT RECEPTOR; SEMAPHORIN 3F; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT7B PROTEIN;

CELL DIFFERENTIATION; CHP GENE; DIENCEPHALON; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DOWN REGULATION; EMBRYO DEVELOPMENT; EPHB1 GENE; FASCICULATION; FIBROBLAST; GENE; GENETIC VARIABILITY; HUMAN; IMMUNOREACTIVITY; MACROPHAGE; MEDIAL FOREBRAIN BUNDLE; MESENCEPHALON; MESOTELENCEPHALIC PATHWAY; NEOCORTEX; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PREFRONTAL CORTEX; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; R RAS GENE; REVIEW; RRAS2 GENE; SEMA5A GENE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TELENCEPHALON; UPREGULATION; WNT SIGNALING PATHWAY;

EID: 84865062405     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2012.00032     Document Type: Review

References (114)

1. Abelson, J. F., Kwan, K. Y., O'Roak, B. J., Baek, D. Y., Stillman, A. A., Morgan, T. M., Mathews, C. A., Pauls, D. L., Rasin, M. R., Gunel, M., Davis, N. R., Ercan-Sencicek, A. G., Guez, D. H., Spertus, J. A., Leckman, J. F., Dure, L. S., Kurlan, R., Singer, H. S., Gilbert, D. L., Farhi, A., Louvi, A., Lifton, R. P., Sestan, N., and State, M. W. (2005). Sequence variants in SLITRK1 are associated with Tourette's syndrome. Science 310, 317-320.
2. Altman, J., and Bayer, S. A. (1981). Development of the brain stem in the rat. V. Thymidine-radiographic study of the time of origin of neurons in the midbrain tegmentum. J. Comp. Neurol. 198, 677-716.
3. Bagri, A., Cheng, H. J., Yaron, A., Pleasure, S. J., and Tessier-Lavigne, M. (2003). Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the Semaphorin family. Cell 113, 285-299.
4. Bagri, A., Marin, O., Plump, A. S., Mak, J., Pleasure, S. J., Rubenstein, J. L. R., and Tessier-Lavigne, M. (2002). Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33, 233-248.
5. Bahi, A., and Dreyer, J. L. (2005). Cocaine-induced expression changes of axon guidance molecules in the adult rat brain. Mol. Cell. Neurosci. 28, 275-291.
6. Baker, K. A., and Mendez, I. (2005). Long distance selective fiber out-growth of transplanted hNT neurons in white matter tracts of the adult rat brain. J. Comp. Neurol. 486, 318-330.
7. Barnes, G., Puranam, R. S., Luo, Y., and McNamara, J. O. (2003). Temporal specific patterns of Semaphorin gene expression in rat brain after kainic acid-induced status epilepticus. Hippocampus 13, 1-20.
8. Bashaw, G. J., and Klein, R. (2010). Signaling from axon guidance receptors. Cold Spring Harb. Perspect. Biol. 2, a001941.
9. Bjorklund, A., Cederfjäll, E. A., and Kirik, D. (2010). Gene therapy for dopamine replacement. Prog. Brain Res. 184, 221-235.
10. Bjorklund, A., Rosenblad, C., Winkler, C., and Kirik, D. (1997). Studies on neuroprotective and regenerative effects of GDNF in a partial lesion model of Parkinson's disease. Neurobiol. Dis. 4, 186-200.
11. Bjorklund, A., and Dunnett, S. B. (2007). Dopamine neuron systems in the brain: an update. Trends Neurosci. 5, 194-202.
12. Blaess, S., Corrales, J. D., and Joyner, A. L. (2006). Sonic hedghog regulates Gli activator and repressor functions with spatial and temporal precision in the mid/hindbrain region. Development 133, 1799-1809.
13. Blakely, B. D., Bye, C. R., Fernando, C. V., Horne, M. K., Macheda, M. L., Stacker, S. A., Arenas, E., and Parish, C. L. (2011). Wnt5a regulates midbrain dopaminergic axon growth and guidance. Plos ONE 3:e18373. doi: 10.1371/journal.pone.0018373
14. Bossers, K., Meerhoff, G., Balesar, R., van Dongen, J. W., Kruse, C. G., Swaab, D. F., and Verhaagen, J. (2009). Analysis of gene expression in Parkinson's disease: possible involvement of neurotrophic support and axon guidance in dopaminergic. Brain Pathol. 19, 91-107.
15. Bouzioukh, F., Daoudal, G., Falk, J., Debanne, D., Rougon, G., and Castellani, V. (2006). Semaphorin3A regulates synaptic function of differentiated hippocampal neurons. Eur. J. Neurosci. 23, 2247-2254.
16. Bundesen, L. Q., Scheel, T. A., Bregman, B. S., and Kromer, L. F. (2003). Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats. J. Neurosci. 27, 7789-7800.
17. Charytoniuk, D., Porcel, B., Rodríguez Gomez, J., Faure, H., Ruat, M., and Traiffort, E. (2002). Sonic Hedgehog signaling in the developing and adult brain. Eur. J. Neurosci. 16, 2351-2357.
18. Chen, L. W., Kuang, F., Wei, L. C., Ding, Y. X., Yung, K. K., and Chan, Y. S. (2011). Potential appliation of induced pluripotent stem cells in cell replacement therapy for Parkinson's disease. CNS Neurol. Disord. Drug Targets 10, 449-458.
19. Cooper, M. A., Kobayashi, K., and Zhou, R. (2009). Ephrin-A5 regulates the formation of the ascending midbrain dopaminergic pathways. Dev. Neurobiol. 69, 36-46.
20. Cord, B. J., Li, J., Works, M., McConnell, S. K., Palmer, T., and Hynes, M. A. (2010). Characterization of axon guidance cue sensitivity of human embryonic stem cell-derived dopaminergic neurons. Mol. Cell. Neurosci. 45, 324-334.
21. Deschamps, C., Faideau, M., Jaber, M., Gaillard, A., and Prestoz, L. (2009). Expression of ephrin-A5 during development and potential involvement in the guidance of the mesostriatal pathway. Exp. Neurol. 219, 466-480.
22. Deschamps, C., Morel, M., Janet, T., Page, G., Jaber, M., Gaillard, A., and Prestoz, L. (2010). Ephrin-A5 protein distribution in the developing mouse brain. BMC Neurosci. 11, 105.
23. Djaldetti, R., Ziv, I., and Melamed, E. (2006). The mystery of motor asymmetry in Parkinson's disease. Lancet Neurol. 5, 796-802.
24. Dugan, J. P., Stratton, A., Riley, H. P., Farmer, W. T., and Mastick, G. S. (2011). Midbrain dopaminergic axons are guided longitudinally through the diencephalon by Slit/Robo signals. Mol. Cell. Neurosci. 46, 347-356.
25. Elstner, M., Morris, C. M., Heim, K., Lichtner, P., Bender, A., Mehta, D., Schulte, C., Sharma, M., Hudson, G., Goldwurm, S., Giovanetti, A., Zeviani, M., Burn, D. J., McKeith, I. G., Perry, R. H., Jaros, E., Krüger, R., Wichmann, H.-E., Schreiber, S., Campbell, H., Wilson, J. F., Wright, A. F., Dunlop, M., Pistis, G., Toniolo, D., Chinnery, P. F., Gasser, T., Klopstock, T., Meitinger, T., Prokisch, H., and Turnbull, D. M. (2009). Single-cell expression profiling of dopaminergic neurons combined with association analysis identifies pyridoxal kinase as Parkinson's disease gene. Ann. Neurol. 66, 792-798.
26. Fabes, J., Anderson, P., Yanez-Munoz, R. J., Thrasher, A., Brennan, C., and Bolsover, S. (2006). Accumulation of the inhibitory receptor EphA4 may prevent regeneration of corticospinal tract axons following lesion. Eur. J. Neurosci. 23, 1721-1730.
27. Fenstermaker, A. G., Prasad, A. A., Bechara, A., Adolfs, Y., Tissir, F., Goffinet, A., Zou, Y., and Pasterkamp, R. J. (2010). Wnt/Planar cell polarity signaling controls the anterior-posterior organization of monoaminergic axons in the brainstem. J. Neurosci. 47, 16053-16064.
28. Flanagan, J. G. (2006). Neural map specification by gradients. Curr. Opin. Neurobiol. 16, 59-66.
29. Flores, C. (2011). Role of netrin-1in the organization and function of the mesocorticolimbic dopamine system. J. Psychiatry Neurosci. 36, 296-310.
30. Gaillard, A., Decressac, M., Frappé, I., Fernagut, P. O., Prestoz, L., Besnard, S., and Jaber, M. (2009). Anatomical and functional reconstruction of the nigrostriatal pathway by intranigral transplants. Neurobiol. Dis. 35, 477-488.
31. Gaillard, A., and Jaber, M. (2011). Rewiring the brain with cell transplantation in Parkinson's disease. Trends Neurosci. 34, 124-133.
32. Gates, M. A., Coupe, V. M., Torres, E. M., Fricker-Gates, R. A., and Dunnett, S. B. (2004). Spatially and temporally restricted chemoattractive and chemorepulsive cues direct the formation of the nigrostriatal circuit. Eur. J. Neurosci. 19, 831-844.
33. Giger, R. J., Cloutier, J. F., Sahay, A., Prinjha, R. K., Levengood, D. V., Moore, S. E., Pickering, S., Simmons, D., Rastan, S., Walsh, F. S., Kolodkin, A. L., Ginty, D. D., and Geppert, M. (2000). Neuropilin-2 is required in vivo for selective axon guidance responses to secreted Semaphorins. Neuron 25, 29-41.
34. Giger, R. J., Hollis, E. R. 2nd, and Tuszynski, M. H. (2010). Guidance molecules in axon regeneration. Cold Spring Harb. Perspect. Biol. 2, a001867.
35. Goldshmit, Y., McLenachan, S., and Turnley, A. (2006). Roles of Eph receptors and ephrins in the normal and damaged adult CNS. Brain Res. Rev. 52, 327-345.
36. Goldshmit, Y., Spanevello, M. D., Tajouri, S., Li, L., Rogers, F., Pearse, M., Galea, M., Bartlett, P. F., Boyd, A. W., and Turnley, A. M. (2011). EphA4 blockers promote axonal regeneration and functional recovery following spinal cord injury in mice. PLoS ONE 6:e24636. doi: 10.1371/journal.pone.0024636
37. Goldshmit, Y., and Bourne, J. (2010). Upregulation of EphA4 on astrocytes potentially mediates astrocytic gliosis after cortical lesion in the Marmoset Monkey. J. Neurotrauma 27, 1321-1332.
38. Grealish, S., Johansson, M. E., Li, M., Kirik, D., Björklund, A., and Thompson, L. H. (2010). The A9 dopamine neuron component in grafts of ventral mesencephalon is an important determinant for recovery of motor function in a rat model of Parkinson's disease. Brain 133, 482-495.
39. Gutekunst, C. A., Stewart, E. N., and Gross, R. E. (2010). Immunohistochemical distribution of plexinA4 in the adult rat central nervous system. Front. Neuroanat. 4:25. doi: 10.3389/fnana.2010.00025
40. Halladay, A. K., Tessarollo, L., Zhou, R., and Wagner, G. C. (2004). Neurochemical and behavioral deficits consequent to expression of a dominant negative EphA5 receptor. Mol. Brain Res. 123, 104-111.
41. Halladay, A. K., Yue, Y., Michna, L., Widmer, D. A. J., Wagner, G. C., and Zhou, R. (2000). Regulation of EphB1 expression by dopamine signaling. Mol. Brain Res. 85, 171-178.
42. Hamasaki, T., Goto, S., Nishikawa, S., and Ushio, Y. (2001). A role of netrin-1 in the formation of the subcortical structure striatum: repulsive action on the migration of late-born striatal neurons. J. Neurosci. 21, 4272-4280.
43. Hammond, R., Blaess, S., and Abeliovich, A. (2009). Sonic Hedgehog is a chemoattractant for midbrain dopaminergic axons. PLoS ONE 4:e7007. doi: 10.1371/ journal.pone.0007007
44. Hernandez-Montiel, H. L., Tamariz, E., Sandoval-Minero, M. T., and Varela-Echavarria, A. (2008). Semaphorins 3A, 3C, and 3F in mesencephalic dopaminergic axon pathfinding. J. Comp. Neurol. 506, 387-397.
45. Herzog, C. D., Brown, L., Gammon, D., Kruegel, B., Lin, R., Wilson, A., Bolton, A., Printz, M., Gasmi, M., Bishop, K. M., Kordower, J. H., and Bartus, R. T. (2009). Expression, bioactivity, and safety 1 year after adeno-associated viral vector type 2-mediated delivery of neurturin to the monkey nigrostriatal system support cere-120 for Parkinson's disease. Neurosurgery 64, 602-612.
46. Hirsch, E., Hu, L. J., Prigent, A., Constantin, B., Agid, Y., Drabkin, H., and Roche, J. (1999). Distribution of Semaphorin IV in adult human brain. Brain Res. 823, 67-79.
47. Holtmaat, A. J., De Winter, F., De Wit, J., Gorter, J. A., da Silva, F. H., and Verhaagen, J. (2002). Semaphorins: contributors to structural stability of hippocampal networks? Prog. Brain Res. 138, 17-38.
48. Hu, Z., Cooper, M., Crockett, D. P., and Zhou, R. (2004). Differentiation of the midbrain dopaminergic pathways during mouse development. J. Comp. Neurol. 476, 301-311.
49. Hynes, M., Porter, J. A., Chiang, C., Chang, D., Tessier-Lavigne, M., Beachy, P. A., and Rosenthal, A. (1995). Induction of midbrain dopaminergic neurons by sonic hedgehog. Neuron 15, 35-44.
50. Janis, L. S., Cassidy, R. M., and Kromer, L. F. (1999). Ephrin-A binding and EphA receptor expression delineate the matrix compartment of the striatum. J. Neurosci. 19, 4962-4971.
51. Jassen, A. K., Yang, H., Miller, G. M., Calder, E., and Madras, B. K. (2006). Receptor regulation of gene expression of axon guidance molecules: implications for adaptation. Mol. Pharmacol. 70, 71-77.
52. Kantor, D. B., Chivatakarn, O., Peer, K. L., Oster, S. F., Inatani, M., Hansen, M. J., Flanagan, J. G., Yamaguchi, Y., Sretavan, D. W., Giger, R. J., and Kolodkin, A. L. (2004). Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44, 961-975.
53. Kawano, H., Horie, M., Honma, S., Kawamura, K., Takeuchi, K., and Kimura, S. (2003). Aberrant trajectory of ascending dopaminergic pathway in mice lacking Nkx2.1. Exp. Neurol. 182, 103-112.
54. Kim, J.-M., Park, S. K., Yang, J. J., Shin, E.-S., Lee, J.-Y., Yun, J. Y., Kim, J. S., Park, S. S., and Jeon, B. S. (2011). SNPs in axon guidance pathway genes and susceptibility for Parkinson's disease in the Korean population. J. Hum. Genet. 56, 125-129.
55. Kolk, S. M., Gunput, R.-A. F., Tran, T. S., van den Heuvel, D. M. A., Prasad, A. A., Hellemons, A. J. C. G. M., Adolfs, Y., Ginty, D. D., Kolodkin, A. L., Burbach, J. P. H., Smidt, M. P., and Pasterkamp, R. J. (2009). Semaphorin 3F is a bifunctional guidance cue for dopaminergic axons and controls their fasciculation, channeling, rostral growth, and intracortical targeting. J. Neurosci. 29, 12542-12557.
56. Kriks, S., Shim, J. W., Piao, J., Ganat, Y. M., Wakeman, D. R., Xie, Z., Carrillo-Reid, L., Auyeung, G., Antonacci, C., Buch, A., Yang, L., Beal, M. F., Surmeier, D. J., Kordower, J. H., Tabar, V., and Studer, L. (2011). Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480, 547-551.
57. Lesnick, T. G., Papapetropoulos, S., Mash, D. C., Ffrench-Mullen, J., Shehadeh, L., de Andrade, M., Henley, J. R., Rocca, W. A., Ahlskog, J. E., and Maraganore, D. M. (2007). A genomic pathway approach to a complex disease: axon guidance and parkinson disease. PLoS Genet. 3:e98. doi: 10.1371/journal.pgen.0030098
58. Li, Y., Rowland, C., Xiromerisiou, G., Lagier, R. J., Schrodi, S. J., Dradiotis, E., Ross, D., Bui, N., Catanese, J., Aggelakis, K., Grupe, A., and Hadjigeorgiou, G. (2008). Neither replication nor simulation supports a role for the axon guidance pathway in the genetics of Parkinson's disease. PLoS ONE 3:e2707. doi: 10.1371/journal.pone.0002707
59. Lin, L., Rao, Y., and Isacson, O. (2005). Netrin-1 and slit-2 regulate and direct neurite growth of ventral midbrain dopaminergic neurons. Mol. Cell. Neurosci. 28, 547-555.
60. Lin, L., and Isacson, O. (2006). Axonal growth regulation of foetal and embryonic stem cellderived dopaminergic neurons by netrin-1 and slits. Stem Cells 24, 2504-2513.
61. Lindvall, O., and Björklund, A. (2004). Cell therapy in Parkinson's disease. NeuroRx 1, 382-393.
62. Lindvall, O., and Björklund, A. (2011). Cell therapeutics in Parkinson's disease. Neurotherapeutics 8, 539-548.
63. Livesey, F. J., and Hunt, S. P. (1997). Netrin and netrin receptor expression in the embryonic mammalian nervous system suggests roles in retinal, striatal, nigral, and cerebellar development. Mol. Cell. Neurosci. 8, 417-429.
64. Malaterre, J., Ramsay, R. G., and Mantamadiotis, T. (2007). Wnt-Frizzled signaling and the many paths to neural development and adult brain homeostasis. Front. Biosci. 12, 492-506.
65. Manitt, C., Labelle-Dumais, C., Eng, C., Grant, A., Mimee, A., Stroh, T., and Flores, C. (2010). Peri-pubertal emergence of UNC-5 homologue expression by dopamine neurons in rodents. PLoS ONE 5:e11463. doi: 10.1371/journal.pone.0011463
66. Manitt, C., Mimee, A., Eng, C., Pokinko, M., Stroh, T., Cooper, H. M., Kolb, B., and Flores, C. (2011). The netrin receptor DCC is required in the pubertal organization of mesocortical dopamine circuitry. J. Neurosci. 31, 8381-8394.
67. Mann, F., Chauvet, S., and Rougon, G. (2007). Semaphorins in development and adult brain: implication for neurological diseases. Prog. Neurobiol. 82, 57-79.
68. Maraganore, D. M., de Andrade, M., Lesnick, T. G., Strain, K. J., Farrer, M. J., Rocca, W. A., Pant, P. V., Frazer, K. A., Cox, D. R., and Ballinger, D. G. (2005). Highresolution whole-genome association study of Parkinson disease. Am. J. Hum. Genet. 77, 685-693.
69. Marchand, R., and Poirier, L. J. (1983). Isthmic origin of neurons of the rat substantia nigra. Neuroscience 9, 373-381.
70. Marillat, V., Cases, O., Nguyen-Ba-Charvet, K. T., Tessier-Lavigne, M., Sotelo, C., and Chédotal, A. (2002). Spatiotemporal expression patterns of slit and robo genes in the rat brain. J. Comp. Neurol. 442, 130-155.
71. Marion, J. F., Yang, C., Caqueret, A., Boucher, F., and Michaud, J. L. (2005). Sim1 and Sim2 are required for the correct targeting of mammillary body axons. Development 132, 5527-5537.
72. Martone, M. E., Holash, J. A., Bayardo, A., Pasquale, E. B., and Ellisman, M. H. (1997). Immunolocalization of the receptor tyrosine kinase EphA4 in the adult rat central nervous system. Brain Res. 771, 238-250.
73. Marín, O., Baker, J., Puelles, P., and Rubenstein, J. L. R. (2002). Patterning of the basal telencephalon and hypothalamus is essential for guidance of cortical projections. Development 129, 761-773.
74. Mendez, I., Sadi, D., and Hong, M. (1996). Reconstruction of the nigrostriatal pathway by simultaneous intrastriatal and intranigral dopaminergic transplants. J. Neurosci. 16, 7216-7227.
75. Mendez, I., and Hong, M. (1997). Reconstruction of the striato-nigro-striatal circuitry by simultaneous double dopaminergic grafts: a tracer study using fluorogold and horseradish peroxidase. Brain Res. 778, 194-205.
76. Migani, P., Bartlett, C., Dunlop, S., Beazley, L., and Rodger, J. (2007). Ephrin-B2 immunoreactivity distribution in adult mouse brain. Brain Res. 28, 60-72.
77. Miyasaki, J. M., Grimes, D., and Lang, A. E. (1999). Acute delirium after withdrawal of amantadine in Parkinson's disease. Neurology 52, 1720-1721.
78. Moreno-Flores, M. T., and Wandosell, F. (1999). Up-regulation of Eph tyrosine kinase receptors after excitotoxic injury in adult hippocampus. Neuroscience 91, 193-201.
79. Nakamura, S.-I., Ito, Y., Shirasaki, R., and Murakami, F. (2000). Local directional cues control growth polarity of dopaminergic axons along the rostrocaudal axis. J. Neurosci. 20, 4112-4119.
80. Olivieri, G., and Miescher, G. C. (1999). Immunohistochemical localization of EphA5 in the adult human central nervous system. J. Histochem. Cytochem. 47, 855-861.
81. Osborne, P. B., Halliday, G. M., Cooper, H. M., and Keast, J. R. (2005). Localization of immunoreactivity for deleted in colorectal cancer (DCC), the receptor for the guidance factor netrin-1, in ventral tier dopamine projection pathways in adult rodents. Neuroscience 131, 671-681.
82. Pasterkamp, R. J., De Winter, F., Holtmaat, A. J. G. D., and Verhaagen, J. (1998). Evidence for a role of the chemorepellent semaphorin III and its receptor neuropilin-1 in the regeneration of primary olfactory axons. J. Neurosci. 18, 9962-9976.
83. Pasterkamp, R. J., Kolk, S. M., Hellemons, A. J. C. G. M., and Kolodkin, A. L. (2007). Expression patterns of semaphorin7A and plexinC1 during rat neural development suggest roles in axon guidance and neuronal migration. BMC Dev. Biol. 7, 98.
84. Pasterkamp, R. J., and Giger, R. J. (2009). Semaphorin function in neural plasticity and disease. Curr. Opin. Neurobiol. 19, 263-274.
85. Rangasamy, S. B., Soderstrom, K., Bakay, R. A., and Kordower, J. H. (2010). Neurotrophic factor therapy for Parkinson's disease. Prog. Brain Res. 184, 237-264.
86. Sancho, R. M., Law, B. M. H., and Harvey, K. (2009). Mutations in the LRRK2 Roc-COR tandem domain link Parkinson's disease to Wnt signaling pathways. Hum. Mol. Genet. 18, 3955-3968.
87. Sawamoto, K., Nakao, N., Kobayashi, K., Matsushita, N., Takahashi, H., Kakishita, K., Yamamoto, A., Yoshizaki, T., Terashima, T., Murakami, F., Itakura, T., and Okano, H. (2001). Visualization, direct isolation, and transplantation of midbrain dopaminergic neurons. Proc. Natl. Acad. Sci. U.S.A. 98, 6423-6428.
88. Shirvan, A., Shina, R., Ziv, I., Melamed, E., and Barzilai, A. (2000). Induction of neuronal apoptosis by Semaphorin3Aderived peptide. Mol. Brain Res. 83, 81-93.
89. Shults, C. W., Albert, L., Kimber, T. A., and Stallcup, W. B. (1992). Mesostriatal dopaminergic axons transiently express high levels of NILE during development. Exp. Neurol. 116, 275-285.
90. Sieber, B. A., Kuzmin, A., Canals, J. M., Danielsson, A., Paratcha, G., Arenas, E., Alberch, J., Ogren, S. O., and Ibáñez, C. F. (2004). Disruption of EphA/ephrin-A signaling in the nigrostriatal system reduces dopaminergic innervation and dissociates behavioral responses to amphetamine and cocaine. Mol. Cell. Neurosci. 26, 418-428.
91. Smidt, M. P., and Burbach, J. P. (2007). How to make a mesodiencephalic dopaminergic neuron. Nat. Rev. Neurosci. 8, 21-32.
92. Specht, L. A., Pickel, V. M., Joh, T. H., and Reis, D. J. (1981a). Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. I. Early ontogeny. J. Comp. Neurol. 199, 233-253.
93. Specht, L. A., Pickel, V. M., Joh, T. H., and Reis, D. J. (1981b). Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. II. Late ontogeny. J. Comp. Neurol. 199, 255-276.
94. Tamariz, E., Díaz-Martínez, N. E., Díaz, N. F., García-Peña, C. M., Velasco, I., and Varela-Echavarría, A. (2010). Axon responses of embryonic stem cell-derived dopaminergic neurons to semaphorins 3A and 3C. J. Neurosci. Res. 88, 971-980.
95. Tang, M., Miyamoto, Y., and Huang, E. J. (2009). Multiple roles of beta-catenin in controlling the neurogenic niche for midbrain dopamine neurons. Development 136, 2027-2038.
96. Thompson, L., Barraud, P., Andersson, E., Kirik, D., and Björklund, A. (2005). Identification of dopaminergic neurons of nigral and ventral tegmental area subtypes in grafts of foetal ventral mesencephalon based on cell morphology, protein expression, and efferent projections. J. Neurosci. 25, 6467-6477.
97. Thompson, L. H., Grealish, S., Kirik, D., and Björklund, A. (2009). Reconstruction of the nigrostriatal dopamine pathway in the adult mouse brain. Eur. J. Neurosci. 30, 625-638.
98. Tissir, F., Bar, I., Jossin, Y., De Backer, O., and Goffinet, A. M. (2005). Protocadherin Celsr3 is crucial in axonal tract development. Nat. Neurosci. 8, 451-457.
99. Torre, E. R., Gutekunst, C.-A., and Gross, R. E. (2010). Expression by midbrain dopamine neurons of Sema3A and 3F receptors is associated with chemorepulsion in vitro but a mild in vivo phenotype. Mol. Cell. Neurosci. 44, 135-153.
100. Tsuchiya, R., Takahashi, K., Liu, F. C., and Takahashi, H. (2009). Aberrant axonal projections from mammillary bodies in Pax6 mutant mice: possible roles of Netrin-1 and Slit 2 in mammillary projections. J. Neurosci. Res. 87, 1620-1633.
101. Vitalis, T., Cases, O., Engelkamp, D., Verney, C., and Price, D. J. (2000). Defects of tyrosine hydroxylaseimmunoreactive neurons in the brains of mice lacking the transcription factor Pax6. J. Neurosci. 20, 6501-6516.
102. Voorn, P., Kalsbeek, A., Jorritsma-Byham, B., and Groenewegen, H. J. (1988). The pre and postnatal development of the dopaminergic cell groups in the ventral mes encephalon and the dopaminergic innervation of the striatum of the rat. Neuroscience 25, 857-887.
103. Wang, Y., Ying, G.-X., Liu, X., Wang, W.-Y., Dong, J.-H., Ni, Z.-M., and Zhou, C.-F. (2005). Induction of ephrin-B1 and EphB receptors during denervation-induced plasticity in the adult mouse hippocampus. Eur. J. Neurosci. 21, 2336-2346.
104. Wehrle, R., Camand, E., Chedotal, A., Sotelo, C., and Dusart, I. (2005). Expression of netrin-1, slit-1 and slit-3 but not of slit-2 after cerebellar and spinal cord lesions. Eur. J. Neurosci. 22, 2134-2144.
105. Wernig, M., Zhao, J. P., Pruszak, J., Hedlund, E., Fu, D., Soldner, F., Broccoli, V., Constantine-Paton, M., Isacson, O., and Jaenisch, R. (2008). Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 105, 5856-5861.
106. Xiao, D., Miller, G. M., Jassen, A., Westmoreland, S. V., Pauley, D., and Madras, B. K. (2006). Ephrin/Eph receptor expression in brain of adult nonhuman primates: implications for neuroadaptation. Brain Res. 1067, 67-77.
107. Xu, B., Goldman, J. S., Rymar, V. V., Forget, C., Lo, P. S., Bull, S. J., Vereker, E., Barker, P. A., Trudeau, L. E., Sadikot, A. F., and Kennedy, T. E. (2010). Critical roles for the netrin receptor deleted in colorectal cancer in dopaminergic neuronal precursor migration, axon guidance, and axon arborization. Neuroscience 169, 932-949.
108. Yamaguchi, Y., and Pasquale, E. B. (2004). Eph receptors in the adult brain. Curr. Opin. Neurobiol. 14, 288-296.
109. Yamauchi, K., Mizushima, S., Tamada, A., Yamamoto, N., Takashima, S., and Murakami, F. (2009). FGF8 signaling regulates growth of midbrain dopaminergic axons by inducing semaphorin 3F. J. Neurosci. 29, 4044-4055.
110. Yasuhara, T., Shingo, T., Kobayashi, K., Takeuchi, A., Yano, A., Muraoka, K., Matsui, T., Miyoshi, Y., Hamada, H., and Date, I. (2004). Neuroprotective effects of vascular endothelial growth factor (VEGF) upon dopaminergic neurons in a rat model of Parkinson's disease. Eur. J. Neurosci. 19, 1494-1504.
111. Yetnikoff, L., Labelle-Dumais, C., and Flores, C. (2007). Regulation of netrin-1 receptors by amphetamine in the adult brain. Neuroscience 150, 764-773.
112. Yue, Y., Chen, Z.-Y., Gale, N. W., Blair-Flynn, J., Hus, T.-J., Yue, X., Cooper, M., Crockett, D. P., Tessarollo, L., and Zhou, R. (2002). Mistargeting hippocampal axons by expression of a truncated Eph receptor. Proc. Natl. Acad. Sci. U.S.A. 99, 10777-10782.
113. Yue, Y., Widmer, D. A., Halladay, A. K., Cerretti, D. P., Wagner, G. C., Dreyer, J. L., and Zhou, R. (1999). Specification of distinct dopaminergic deural pathways: roles of the Eph family receptor EphB1 and ligand Ephrin-B2. J. Neurosci. 19, 2090-2101.
114. Zhou, F. C., and Chiang, Y. H. (1995). Excitochemical-induced trophic bridging directs axonal growth of transplanted neurons to distal target. Cell Transplant. 4, 103-112.