Canonical BMP-Smad signalling promotes neurite growth in rat midbrain dopaminergic neurons

NeuroMolecular Medicine

Volumn 16, Issue 2, 2014, Pages 473-489

  Hegarty, Shane V ^a   Collins, Louise M ^a   Gavin, Aisling M ^a   Roche, Sarah L ^a   Wyatt, Sean L ^b   Sullivan, Aideen M ^a   O'Keeffe, Gerard W ^a,c  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c Irish Centre for Fetal and Neonatal Translational Research   (Ireland)

Author keywords

BMP receptor; BMP2; Dopaminergic neurons; GDF5; Neurite growth; Smad signalling; Ventral midbrain

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; GROWTH DIFFERENTIATION FACTOR 5; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; SMALL INTERFERING RNA; (6-(4-(2-PIPERIDIN-1-YLETHOXY)PHENYL))-3-PYRIDIN-4-YLPYRAZOLO(1,5-A)PYRIMIDINE; BMP2 PROTEIN, HUMAN; BMP2 PROTEIN, RAT; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; CARRIER PROTEIN; GDF5 PROTEIN, RAT; NOGGIN PROTEIN; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; RECOMBINANT PROTEIN; SMAD PROTEIN; TYROSINE 3 MONOOXYGENASE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; LIGAND BINDING; MESENCEPHALON; MOLECULAR DYNAMICS; NERVE FIBER GROWTH; NEUROMODULATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; EMBRYOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; NEURITE; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SUBSTANTIA NIGRA; ULTRASTRUCTURE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; CARRIER PROTEINS; CELLS, CULTURED; CORPUS STRIATUM; DOPAMINERGIC NEURONS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH DIFFERENTIATION FACTOR 5; MESENCEPHALON; NEURITES; NEUROGENESIS; PYRAZOLES; PYRIMIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SMAD PROTEINS; SUBSTANTIA NIGRA; TRANSFECTION; TYROSINE 3-MONOOXYGENASE;

EID: 84901362605     PISSN: 15351084     EISSN: 15591174     Source Type: Journal    
DOI: 10.1007/s12017-014-8299-5     Document Type: Article

References (111)

1. Agius, E., Decker, Y., Soukkarieh, C., Soula, C., & Cochard, P. (2010). Role of BMPs in controlling the spatial and temporal origin of GFAP astrocytes in the embryonic spinal cord. Development Biology, 344(2), 611-620.
2. Allen © 2012 Allen Institute for Brain Science. Allen Mouse Brain Atlas [Internet]. Available from: http://mouse.brain-map.org/.
3. Andrews, Z. B., Zhao, H., Frugier, T., Meguro, R., Grattan, D. R., Koishi, K., et al. (2006). Transforming growth factor beta2 haploinsufficient mice develop age-related nigrostriatal dopamine deficits. Neurobiology of Diseases, 21(3), 568-575.
4. Bagri, A., Marin, O., Plump, A. S., Mak, J., Pleasure, S. J., Rubenstein, J. L., et al. (2002). Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron, 33(2), 233-248.
5. Barnett, M. W., Fisher, C. E., Perona-Wright, G., & Davies, J. A. (2002). Signalling by glial cell line-derived neurotrophic factor (GDNF) requires heparan sulphate glycosaminoglycan. Journal of Cell Science, 115(Pt 23), 4495-4503.
6. Bjorklund, A., & Dunnett, S. B. (2007). Dopamine neuron systems in the brain: An update. Trends in Neurosciences, 30(5), 194-202.
7. Blum, M. (1998). A null mutation in TGF-alpha leads to a reduction in midbrain dopaminergic neurons in the substantia nigra. Nature Neuroscience, 1(5), 374-377.
8. Boger, H. A., Middaugh, L. D., Huang, P., Zaman, V., Smith, A. C., Hoffer, B. J., et al. (2006). A partial GDNF depletion leads to earlier age-related deterioration of motor function and tyrosine hydroxylase expression in the substantia nigra. Experimental Neurology, 202(2), 336-347.
9. Bonnamain, V., Neveu, I., & Naveilhan, P. (2012). Neural stem/progenitor cells as a promising candidate for regenerative therapy of the central nervous system. Frontiers in Cellular Neuroscience, 6, 17.
10. Bovolenta, P. (2005). Morphogen signaling at the vertebrate growth cone: A few cases or a general strategy? Journal of Neurobiology, 64(4), 405-416.
11. Burke, R. E. (2003). Postnatal developmental programmed cell death in dopamine neurons. Annals of the New York Academy of Sciences, 991, 69-79.
12. Butler, S. J., & Dodd, J. (2003). A role for BMP heterodimers in roof plate-mediated repulsion of commissural axons. Neuron, 38(3), 389-401.
13. Calo, L., Spillantini, M., Nicoletti, F., & Allen, N. D. (2005). Nurr1 co-localizes with EphB1 receptors in the developing ventral midbrain, and its expression is enhanced by the EphB1 ligand, ephrinB2. Journal of Neurochemistry, 92(2), 235-245.
14. Chalazonitis, A., D'Autreaux, F., Guha, U., Pham, T. D., Faure, C., Chen, J. J., et al. (2004). Bone morphogenetic protein-2 and -4 limit the number of enteric neurons but promote development of a TrkC-expressing neurotrophin-3-dependent subset. Journal of Neuroscience, 24(17), 4266-4282.
15. Chalazonitis, A., D'Autreaux, F., Pham, T. D., Kessler, J. A., & Gershon, M. D. (2011). Bone morphogenetic proteins regulate enteric gliogenesis by modulating ErbB3 signaling. Development Biology, 350(1), 64-79.
16. Chalazonitis, A., & Kessler, J. A. (2012). Pleiotropic effects of the bone morphogenetic proteins on development of the enteric nervous system. Developmental Neurobiology, 72(6), 843-856.
17. Chen, H. L., Lein, P. J., Wang, J. Y., Gash, D., Hoffer, B. J., & Chiang, Y. H. (2003). Expression of bone morphogenetic proteins in the brain during normal aging and in 6-hydroxydopamine-lesioned animals. Brain Research, 994(1), 81-90.
18. Chizhikov, V. V., & Millen, K. J. (2005). Roof plate-dependent patterning of the vertebrate dorsal central nervous system. Development Biology, 277(2), 287-295.
19. Chou, J., Harvey, B. K., Ebendal, T., Hoffer, B., & Wang, Y. (2008). Nigrostriatal alterations in bone morphogenetic protein receptor II dominant negative mice. Acta Neurochirurgica. Supplementum, 101, 93-98.
20. Collins, L. M., O'Keeffe, G. W., Long-Smith, C. M., Wyatt, S. L., Sullivan, A. M., Toulouse, A., et al. (2013). Mitogen-activated protein kinase phosphatase (MKP)-1 as a neuroprotective agent: Promotion of the morphological development of midbrain dopaminergic neurons. NeuroMolecular Medicine, 15(2), 435-446.
21. Cooper, M. A., Kobayashi, K., & Zhou, R. (2009). Ephrin-A5 regulates the formation of the ascending midbrain dopaminergic pathways. Developmental Neurobiology, 69(1), 36-46.
22. Crampton, S. J., Collins, L. M., Toulouse, A., Nolan, Y. M., & O'Keeffe, G. W. (2012). Exposure of foetal neural progenitor cells to IL-1beta impairs their proliferation and alters their differentiation: A role for maternal inflammation? Journal of Neurochemistry, 120(6), 964-973.
23. Crossley, P. H., & Martin, G. R. (1995). The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development, 121(2), 439-451.
24. Dahlstroem, A., & Fuxe, K. (1964). Evidence for the existence of monoamine-containing neurons in the bentral nervous syste, I. Demonstrations of monoamines in the cell bodies of brain stem neurons. Acta Physiologica Scandinavica. Supplementum., 232, 231-255.
25. De Feo, D., Merlini, A., Laterza, C., & Martino, G. (2012). Neural stem cell transplantation in central nervous system disorders: From cell replacement to neuroprotection. Current Opinion in Neurology, 25(3), 322-333.
26. Dent, E. W., Gupton, S. L., & Gertler, F. B. (2011). The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb Perspect Biol, 3(3).
27. Dugan, J. P., Stratton, A., Riley, H. P., Farmer, W. T., & Mastick, G. S. (2011). Midbrain dopaminergic axons are guided longitudinally through the diencephalon by Slit/Robo signals. Molecular and Cellular Neuroscience, 46(1), 347-356.
28. Egea, J., & Klein, R. (2007). Bidirectional Eph-ephrin signaling during axon guidance. Trends in Cell Biology, 17(5), 230-238.
29. Espejo, M., Cutillas, B., Ventura, F., & Ambrosio, S. (1999). Exposure of foetal mesencephalic cells to bone morphogenetic protein-2 enhances the survival of dopaminergic neurones in rat striatal grafts. Neuroscience Letters, 275(1), 13-16.
30. Flores, C., Manitt, C., Rodaros, D., Thompson, K. M., Rajabi, H., Luk, K. C., et al. (2005). Netrin receptor deficient mice exhibit functional reorganization of dopaminergic systems and do not sensitize to amphetamine. Molecular Psychiatry, 10(6), 606-612.
31. Gates, M. A., Coupe, V. M., Torres, E. M., Fricker-Gates, R. A., & Dunnett, S. B. (2004). Spatially and temporally restricted chemoattractive and chemorepulsive cues direct the formation of the nigro-striatal circuit. European Journal of Neuroscience, 19(4), 831-844.
32. Gates, M. A., Torres, E. M., White, A., Fricker-Gates, R. A., & Dunnett, S. B. (2006). Re-examining the ontogeny of substantia nigra dopamine neurons. European Journal of Neuroscience, 23(5), 1384-1390.
33. German, D. C., Schlusselberg, D. S., & Woodward, D. J. (1983). Three-dimensional computer reconstruction of midbrain dopaminergic neuronal populations: From mouse to man. Journal of Neural Transmission, 57(4), 243-254.
34. Gratacos, E., Checa, N., Perez-Navarro, E., & Alberch, J. (2001). Brain-derived neurotrophic factor (BDNF) mediates bone morphogenetic protein-2 (BMP-2) effects on cultured striatal neurones. Journal of Neurochemistry, 79(4), 747-755.
35. Gratacos, E., Gavalda, N., & Alberch, J. (2002). Bone morphogenetic protein-6 is a neurotrophic factor for calbindin-positive striatal neurons. Journal of Neuroscience Research, 70(5), 638-644.
36. Groppe, J., Greenwald, J., Wiater, E., Rodriguez-Leon, J., Economides, A. N., Kwiatkowski, W., et al. (2002). Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature, 420(6916), 636-642.
37. Gutierrez, H., & Davies, A. M. (2007). A fast and accurate procedure for deriving the Sholl profile in quantitative studies of neuronal morphology. Journal of Neuroscience Methods, 163(1), 24-30.
38. Halladay, A. K., Tessarollo, L., Zhou, R., & Wagner, G. C. (2004). Neurochemical and behavioral deficits consequent to expression of a dominant negative EphA5 receptor. Molecular Brain Research, 123(1-2), 104-111.
39. Hazen, V. M., Andrews, M. G., Umans, L., Crenshaw, E. B, 3rd, Zwijsen, A., & Butler, S. J. (2012). BMP receptor-activated Smads confer diverse functions during the development of the dorsal spinal cord. Development Biology, 367(2), 216-227.
40. Hazen, V. M., Phan, K. D., Hudiburgh, S., & Butler, S. J. (2011). Inhibitory Smads differentially regulate cell fate specification and axon dynamics in the dorsal spinal cord. Development Biology, 356(2), 566-575.
41. Hedlund, E., & Perlmann, T. (2009). Neuronal cell replacement in Parkinson's disease. Journal of Internal Medicine, 266(4), 358-371.
42. Hegarty, S. V., O'Keeffe, G. W., & Sullivan, A. M. (2013a). BMP-Smad 1/5/8 signalling in the development of the nervous system. Progress in Neurobiology, 109C, 28-41.
43. Hegarty, S. V., Sullivan, A. M., & O'Keeffe, G. W. (2013b). BMP2 and GDF5 induce neuronal differentiation through a Smad dependant pathway in a model of human midbrain dopaminergic neurons. Molecular and Cellular Neuroscience, 56C, 263-271.
44. Hegarty, S. V., Sullivan, A. M., & O'Keeffe, G. W. (2013c). Midbrain dopaminergic neurons: A review of the molecular circuitry that regulates their development. Development Biology, 379(2), 123-138.
45. Hegarty, S. V., Sullivan, A. M., & O'Keeffe, G. W. (2014). Roles for the TGFβ superfamily in the development and survival of midbrain dopaminergic neurons. Molecular Neurobiology,. doi: 10.1007/s12035-014-8639-3.
46. Hernandez-Montiel, H. L., Tamariz, E., Sandoval-Minero, M. T., & Varela-Echavarria, A. (2008). Semaphorins 3A, 3C, and 3F in mesencephalic dopaminergic axon pathfinding. Journal of Comparative Neurology, 506(3), 387-397.
47. Hurley, F. M., Costello, D. J., & Sullivan, A. M. (2004). Neuroprotective effects of delayed administration of growth/differentiation factor-5 in the partial lesion model of Parkinson's disease. Experimental Neurology, 185(2), 281-289.
48. Hynes, M., Porter, J. A., Chiang, C., Chang, D., Tessier-Lavigne, M., Beachy, P. A., et al. (1995). Induction of midbrain dopaminergic neurons by Sonic hedgehog. Neuron, 15(1), 35-44.
49. Iwase, T., Jung, C. G., Bae, H., Zhang, M., & Soliven, B. (2005). Glial cell line-derived neurotrophic factor-induced signaling in Schwann cells. Journal of Neurochemistry, 94(6), 1488-1499.
50. Jackson-Lewis, V., Vila, M., Djaldetti, R., Guegan, C., Liberatore, G., Liu, J., et al. (2000). Developmental cell death in dopaminergic neurons of the substantia nigra of mice. Journal of Comparative Neurology, 424(3), 476-488.
51. Jordan, J., Bottner, M., Schluesener, H. J., Unsicker, K., & Krieglstein, K. (1997). Bone morphogenetic proteins: Neurotrophic roles for midbrain dopaminergic neurons and implications of astroglial cells. European Journal of Neuroscience, 9(8), 1699-1709.
52. Koenig, B. B., Cook, J. S., Wolsing, D. H., Ting, J., Tiesman, J. P., Correa, P. E., et al. (1994). Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Molecular and Cellular Biology, 14(9), 5961-5974.
53. Kolk, S. M., Gunput, R. A., Tran, T. S., van den Heuvel, D. M., Prasad, A. A., Hellemons, A. J., et al. (2009). Semaphorin 3F is a bifunctional guidance cue for dopaminergic axons and controls their fasciculation, channeling, rostral growth, and intracortical targeting. Journal of Neuroscience, 29(40), 12542-12557.
54. Krieglstein, K., Suter-Crazzolara, C., Hotten, G., Pohl, J., & Unsicker, K. (1995). Trophic and protective effects of growth/differentiation factor 5, a member of the transforming growth factor-beta superfamily, on midbrain dopaminergic neurons. Journal of Neuroscience Research, 42(5), 724-732.
55. Lauder, J. M., & Bloom, F. E. (1974). Ontogeny of monoamine neurons in the locus coeruleus, Raphe nuclei and substantia nigra of the rat. I. Cell differentiation. Journal of Comparative Neurology, 155(4), 469-481.
56. Lees, A. J., Hardy, J., & Revesz, T. (2009). Parkinson's disease. Lancet, 373(9680), 2055-2066.
57. Lein, P., Johnson, M., Guo, X., Rueger, D., & Higgins, D. (1995). Osteogenic protein-1 induces dendritic growth in rat sympathetic neurons. Neuron, 15(3), 597-605.
58. Li, W., & LoTurco, J. J. (2000). Noggin is a negative regulator of neuronal differentiation in developing neocortex. Developmental Neuroscience, 22(1-2), 68-73.
59. Lin, L., Rao, Y., & Isacson, O. (2005). Netrin-1 and slit-2 regulate and direct neurite growth of ventral midbrain dopaminergic neurons. Molecular and Cellular Neuroscience, 28(3), 547-555.
60. Liu, A., & Joyner, A. L. (2001). EN and GBX2 play essential roles downstream of FGF8 in patterning the mouse mid/hindbrain region. Development, 128(2), 181-191.
61. Lopez-Bendito, G., Flames, N., Ma, L., Fouquet, C., Di Meglio, T., Chedotal, A., et al. (2007). Robo1 and Robo2 cooperate to control the guidance of major axonal tracts in the mammalian forebrain. Journal of Neuroscience, 27(13), 3395-3407.
62. Lumsden, A., & Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science, 274(5290), 1109-1115.
63. Manitt, C., Mimee, A., Eng, C., Pokinko, M., Stroh, T., Cooper, H. M., et al. (2011). The netrin receptor DCC is required in the pubertal organization of mesocortical dopamine circuitry. Journal of Neuroscience, 31(23), 8381-8394.
64. Miyazono, K., Kamiya, Y., & Morikawa, M. (2010). Bone morphogenetic protein receptors and signal transduction. Journal of Biochemistry, 147(1), 35-51.
65. Monteiro, R. M., de Sousa Lopes, S. M., Bialecka, M., de Boer, S., Zwijsen, A., & Mummery, C. L. (2008). Real time monitoring of BMP Smads transcriptional activity during mouse development. Genesis, 46(7), 335-346.
66. Nakamura, S., Ito, Y., Shirasaki, R., & Murakami, F. (2000). Local directional cues control growth polarity of dopaminergic axons along the rostrocaudal axis. Journal of Neuroscience, 20(11), 4112-4119.
67. Niere, M., Braun, B., Gass, R., Sturany, S., & Volkmer, H. (2006). Combination of engineered neural cell adhesion molecules and GDF-5 for improved neurite extension in nerve guide concepts. Biomaterials, 27(18), 3432-3440.
68. Nishitoh, H., Ichijo, H., Kimura, M., Matsumoto, T., Makishima, F., Yamaguchi, A., et al. (1996). Identification of type I and type II serine/threonine kinase receptors for growth/differentiation factor-5. Journal of Biological Chemistry, 271(35), 21345-21352.
69. O'Keeffe, G. W., Dockery, P., & Sullivan, A. M. (2004a). Effects of growth/differentiation factor 5 on the survival and morphology of embryonic rat midbrain dopaminergic neurones in vitro. Journal of Neurocytology, 33(5), 479-488.
70. O'Keeffe, G. W., Hanke, M., Pohl, J., & Sullivan, A. M. (2004b). Expression of growth differentiation factor-5 in the developing and adult rat brain. Developmental Brain Research, 151(1-2), 199-202.
71. Oo, T. F., & Burke, R. E. (1997). The time course of developmental cell death in phenotypically defined dopaminergic neurons of the substantia nigra. Developmental Brain Research, 98(2), 191-196.
72. Orlacchio, A., Bernardi, G., & Martino, S. (2010). Stem cells and neurological diseases. Discovery Medicine, 9(49), 546-553.
73. Orme, R. P., Bhangal, M. S., & Fricker, R. A. (2013). Calcitriol imparts neuroprotection in vitro to midbrain dopaminergic neurons by upregulating GDNF expression. PLoS ONE, 8(4), e62040.
74. O'Sullivan, D. B., Harrison, P. T., & Sullivan, A. M. (2010). Effects of GDF5 overexpression on embryonic rat dopaminergic neurones in vitro and in vivo. Journal of Neural Transmission, 117(5), 559-572.
75. Pakkenberg, B., Moller, A., Gundersen, H. J., Mouritzen Dam, A., & Pakkenberg, H. (1991). The absolute number of nerve cells in substantia nigra in normal subjects and in patients with Parkinson's disease estimated with an unbiased stereological method. Journal of Neurology, Neurosurgery and Psychiatry, 54(1), 30-33.
76. Parikh, P., Hao, Y., Hosseinkhani, M., Patil, S. B., Huntley, G. W., Tessier-Lavigne, M., et al. (2011). Regeneration of axons in injured spinal cord by activation of bone morphogenetic protein/Smad1 signaling pathway in adult neurons. Proceedings of the National Academy of Sciences of the United States of America, 108(19), E99-E107.
77. Paxinos, G., & Watson, C. (1988). The rat brain in stereotaxic coordinates. San Diego: Academic Press.
78. Phan, K. D., Hazen, V. M., Frendo, M., Jia, Z., & Butler, S. J. (2010). The bone morphogenetic protein roof plate chemorepellent regulates the rate of commissural axonal growth. Journal of Neuroscience, 30(46), 15430-15440.
79. Reiriz, J., Espejo, M., Ventura, F., Ambrosio, S., & Alberch, J. (1999). Bone morphogenetic protein-2 promotes dissociated effects on the number and differentiation of cultured ventral mesencephalic dopaminergic neurons. Journal of Neurobiology, 38(2), 161-170.
80. Round, J., & Stein, E. (2007). Netrin signaling leading to directed growth cone steering. Current Opinion in Neurobiology, 17(1), 15-21.
81. Sgado, P., Ferretti, E., Grbec, D., Bozzi, Y., & Simon, H. H. (2012). The atypical homeoprotein Pbx1a participates in the axonal pathfinding of mesencephalic dopaminergic neurons. Neural Development, 7, 24.
82. Shi, Y., & Massague, J. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell, 113(6), 685-700.
83. Sieber, C., Kopf, J., Hiepen, C., & Knaus, P. (2009). Recent advances in BMP receptor signaling. Cytokine & Growth Factor Reviews, 20(5-6), 343-355.
84. Sieber, B. A., Kuzmin, A., Canals, J. M., Danielsson, A., Paratcha, G., Arenas, E., et al. (2004). Disruption of EphA/ephrin-a signaling in the nigrostriatal system reduces dopaminergic innervation and dissociates behavioral responses to amphetamine and cocaine. Molecular and Cellular Neuroscience, 26(3), 418-428.
85. Smith, W. C., & Harland, R. M. (1992). Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell, 70(5), 829-840.
86. Soderstrom, S., & Ebendal, T. (1999). Localized expression of BMP and GDF mRNA in the rodent brain. Journal of Neuroscience Research, 56(5), 482-492.
87. Specht, L. A., Pickel, V. M., Joh, T. H., & Reis, D. J. (1981a). Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. I. Early ontogeny. Journal of Comparative Neurology, 199(2), 233-253.
88. Specht, L. A., Pickel, V. M., Joh, T. H., & Reis, D. J. (1981b). Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. II. Late ontogeny. Journal of Comparative Neurology, 199(2), 255-276.
89. Storm, E. E., Huynh, T. V., Copeland, N. G., Jenkins, N. A., Kingsley, D. M., & Lee, S. J. (1994). Limb alterations in brachypodism mice due to mutations in a new member of the TGF beta-superfamily. Nature, 368(6472), 639-643.
90. Sullivan, A. M., & O'Keeffe, G. W. (2005). The role of growth/differentiation factor 5 (GDF5) in the induction and survival of midbrain dopaminergic neurones: Relevance to Parkinson's disease treatment. Journal of Anatomy, 207(3), 219-226.
91. Sullivan, A. M., Opacka-Juffry, J., Hotten, G., Pohl, J., & Blunt, S. B. (1997). Growth/differentiation factor 5 protects nigrostriatal dopaminergic neurones in a rat model of Parkinson's disease. Neuroscience Letters, 233(2-3), 73-76.
92. Sullivan, A. M., Opacka-Juffry, J., Pohl, J., & Blunt, S. B. (1999). Neuroprotective effects of growth/differentiation factor 5 depend on the site of administration. Brain Research, 818(1), 176-179.
93. Sullivan, A. M., Pohl, J., & Blunt, S. B. (1998). Growth/differentiation factor 5 and glial cell line-derived neurotrophic factor enhance survival and function of dopaminergic grafts in a rat model of Parkinson's disease. European Journal of Neuroscience, 10(12), 3681-3688.
94. Sullivan, A. M., & Toulouse, A. (2011). Neurotrophic factors for the treatment of Parkinson's disease. Cytokine & Growth Factor Reviews, 22(3), 157-165.
95. Tamariz, E., Diaz-Martinez, N. E., Diaz, N. F., Garcia-Pena, C. M., Velasco, I., & Varela-Echavarria, A. (2010). Axon responses of embryonic stem cell-derived dopaminergic neurons to semaphorins 3A and 3C. Journal of Neuroscience Research, 88(5), 971-980.
96. ten Dijke, P., Yamashita, H., Sampath, T. K., Reddi, A. H., Estevez, M., Riddle, D. L., et al. (1994). Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. Journal of Biological Chemistry, 269(25), 16985-16988.
97. Torre, E. R., Gutekunst, C. A., & 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. Molecular and Cellular Neuroscience, 44(2), 135-153.
98. Toulouse, A., & Sullivan, A. M. (2008). Progress in Parkinson's disease-where do we stand? Progress in Neurobiology, 85(4), 376-392.
99. Ulloa, F., & Briscoe, J. (2007). Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle, 6(21), 2640-2649.
100. Van den Heuvel, D. M., & Pasterkamp, R. J. (2008). Getting connected in the dopamine system. Progress in Neurobiology, 85(1), 75-93.
101. Verney, C. (1999). Distribution of the catecholaminergic neurons in the central nervous system of human embryos and fetuses. Microscopy Research and Technique, 46(1), 24-47.
102. Vitalis, T., Cases, O., Engelkamp, D., Verney, C., & Price, D. J. (2000). Defect of tyrosine hydroxylase-immunoreactive neurons in the brains of mice lacking the transcription factor Pax6. Journal of Neuroscience, 20(17), 6501-6516.
103. Voorn, P., Kalsbeek, A., Jorritsma-Byham, B., & Groenewegen, H. J. (1988). The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat. Neuroscience, 25(3), 857-887.
104. Wen, Z., Han, L., Bamburg, J. R., Shim, S., Ming, G. L., & Zheng, J. Q. (2007). BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. Journal of Cell Biology, 178(1), 107-119.
105. Wood, T. K., McDermott, K. W., & Sullivan, A. M. (2005). Differential effects of growth/differentiation factor 5 and glial cell line-derived neurotrophic factor on dopaminergic neurons and astroglia in cultures of embryonic rat midbrain. Journal of Neuroscience Research, 80(6), 759-766.
106. Xu, B., Goldman, J. S., Rymar, V. V., Forget, C., Lo, P. S., Bull, S. J., et al. (2010). Critical roles for the netrin receptor deleted in colorectal cancer in dopaminergic neuronal precursor migration, axon guidance, and axon arborization. Neuroscience, 169(2), 932-949.
107. Yamashita, H., Ten Dijke, P., Heldin, C. H., & Miyazono, K. (1996). Bone morphogenetic protein receptors. Bone, 19(6), 569-574.
108. Yamauchi, K., Phan, K. D., & Butler, S. J. (2008). BMP type I receptor complexes have distinct activities mediating cell fate and axon guidance decisions. Development, 135(6), 1119-1128.
109. Yu, P. B., Hong, C. C., Sachidanandan, C., Babitt, J. L., Deng, D. Y., Hoyng, S. A., et al. (2008). Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nature Chemical Biology, 4(1), 33-41.
110. Yue, Y., Widmer, D. A., Halladay, A. K., Cerretti, D. P., Wagner, G. C., Dreyer, J. L., et al. (1999). Specification of distinct dopaminergic neural pathways: Roles of the Eph family receptor EphB1 and ligand ephrin-B2. Journal of Neuroscience, 19(6), 2090-2101.
111. Zou, Y., & Lyuksyutova, A. I. (2007). Morphogens as conserved axon guidance cues. Current Opinion in Neurobiology, 17(1), 22-28.