Molecular mechanisms underlying midbrain dopamine neuron development and function

European Journal of Pharmacology

Volumn 480, Issue 1-3, 2003, Pages 75-88

  Smidt, Marten P ^a   Smits, Simone M ^a   Burbach, J Peter H ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Development; Dopamine; Dopaminergic; Mesencephalic; Midbrain; Pitx3

Indexed keywords

DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; DOPAMINE 5 RECEPTOR; DOPAMINE TRANSPORTER; TYROSINE 3 MONOOXYGENASE;

BRAIN DEVELOPMENT; BRAIN FUNCTION; CONFERENCE PAPER; DOPAMINE METABOLISM; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; EMOTION; GENETIC DISORDER; GENETIC HETEROGENEITY; HOMEOSTASIS; HUMAN; KNOCKOUT MOUSE; MESENCEPHALON; MOVEMENT (PHYSIOLOGY); NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

EID: 0242499436     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2003.08.094     Document Type: Conference Paper

References (96)

1. Acampora D., Simeone A. The TINS Lecture. Understanding the roles of Otx1 and Otx2 in the control of brain morphogenesis. Trends Neurosci. 22:1999;116-122.
2. Acampora D., Mazan S., Lallemand Y., Avantaggiato V., Maury M., Simeone A., Brulet P. Forebrain and midbrain regions are deleted in Otx2-/- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development. 121:1995;3279-3290.
3. Accili D., Fishburn C.S., Drago J., Steiner H., Lachowicz J.E., Park B.H., Gauda E.B., Lee E.J., Cool M.H., Sibley D.R., Gerfen C.R., Westphal H., Fuchs S. A targeted mutation of the D3 dopamine receptor gene is associated with hyperactivity in mice. Proc. Natl. Acad. Sci. U. S. A. 93:1996;1945-1949.
4. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 12:1989;366-375.
5. Andén N.E., Carlsson A., Dahlström A.et al. Demonstration and mapping out of nigro-neostriatal dopamine neurons. Life Sci. 3:1964;523-530.
6. Andén N.E., Fuxe K., Hamberger B., Hokfelt T. A quantitative study on the nigro-neostriatal dopamine neuron system in the rat. Acta Physiol. Scand. 67:1966;306-312.
7. Baik J.H., Picetti R., Saiardi A., Thiriet G., Dierich A., Depaulis A., Le Meur M., Borrelli E. Parkinsonian-like locomotor impairment in mice lacking dopamine D2 receptors. Nature. 377:1995;424-428.
8. Barbeau A., Sourkes T.L., Murphy G.F. Les catecholamines dans la maladie de Parkinson. Ajuriaguerra J. Monoamines et Système Nerveux Central. Symposium Bel-Air, Geneva:1962;247-262 Georg and Co. Geneva.
9. Bertler A., Rosengrens E. Occurrence and distribution of dopamine in brain and other tissues. Experientia. 15:1959;1-3.
10. Bezard E., Gross C.E., Fournier M.C., Dovero S., Bloch B., Jaber M. Absence of MPTP-induced neuronal death in mice lacking the dopamine transporter. Exp. Neurol. 155:1999;268-273.
11. Boulay D., Depoortere R., Perrault G., Borrelli E., Sanger D.J. Dopamine D2 receptor knock-out mice are insensitive to the hypolocomotor and hypothermic effects of dopamine D2/D3 receptor agonists. Neuropharmacology. 38:1999;1389-1396.
12. Broccoli V., Boncinelli E., Wurst W. The caudal limit of Otx2 expression positions the isthmic organizer. Nature. 401:1999;164-168.
13. Carlsson A. The occurrence, distribution and physiological role of catecholamines in the nervous system. Pharmacol. Rev. 11:1959;490-493.
14. Castillo S.O., Baffi J.S., Palkovits M., Goldstein D.S., Kopin I.J., Witta J., Magnuson M.A., Nikodem V.M. Dopamine biosynthesis is selectively abolished in substantia Nigra/Ventral tegmental area but not in hypothalamic neurons in mice with targeted disruption of the Nurr1 gene. Mol. Cell. Neurosci. 11:1998;36-46.
15. Chen H., Lun Y., Ovchinnikov D., Kokubo H., Oberg K.C., Pepicelli C.V., Gan L., Lee B., Johnson R.L. Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nat. Genet. 19:1998;51-55.
16. Clifford J.J., Tighe O., Croke D.T., Sibley D.R., Drago J., Waddington J.L. Topographical evaluation of the phenotype of spontaneous behaviour in mice with targeted gene deletion of the D1A dopamine receptor: paradoxical elevation of grooming syntax. Neuropharmacology. 37:1998;1595-1602.
17. Costall B., Naylor R.J., Nohria V. Differential actions of typical and atypical neuroleptic agents on two behavioural effects of apomorphine in the mouse [proceedings]. Br. J. Pharmacol. 63:1978;381-382.
18. Dahlström A., Fuxe K. Evidence for the existence of monoamine-containing neurons in the central nervous system: I. Demonstration of monoamines in the cell bodies of brian stem neurones. Acta Physiol. Scand. 62:1964;1-55.
19. Danielian P.S., McMahon A.P. Engrailed-1 as a target of the Wnt-1 signalling pathway in vertebrate midbrain development. Nature. 383:1996;332-334.
20. Dickinson S.D., Sabeti J., Larson G.A., Giardina K., Rubinstein M., Kelly M.A., Grandy D.K., Low M.J., Gerhardt G.A., Zahniser N.R. Dopamine D2 receptor-deficient mice exhibit decreased dopamine transporter function but no changes in dopamine release in dorsal striatum. J. Neurochem. 72:1999;148-156.
21. Drago J., Gerfen C.R., Lachowicz J.E., Steiner H., Hollon T.R., Love P.E., Ooi G.T., Grinberg A., Lee E.J., Huang S.P. Altered striatal function in a mutant mouse lacking D1A dopamine receptors. Proc. Natl. Acad. Sci. U. S. A. 91:1994;12564-12568.
22. Drago J., Gerfen C.R., Westphal H., Steiner H. D1 dopamine receptor-deficient mouse: cocaine-induced regulation of immediate-early gene and substance P expression in the striatum. Neuroscience. 74:1996;813-823.
23. Drago F., Contarino A., Busa L. The expression of neuropeptide-induced excessive grooming behavior in dopamine D1 and D2 receptor-deficient mice. Eur. J. Pharmacol. 365:1999;125-131.
24. Dreyer S.D., Zhou G., Baldini A., Winterpacht A., Zabel B., Cole W., Johnson R.L., Lee B. Mutations in LMX1B cause abnormal skeletal patterning and renal dysplasia in nail patella syndrome. Nat. Genet. 19:1998;47-50.
25. Drouin J., Lamolet B., Lamonerie T., Lanctot C., Tremblay J.J. The PTX family of homeodomain transcription factors during pituitary developments. Mol. Cell. Endocrinol. 140:1998;31-36.
26. Dulawa S.C., Grandy D.K., Low M.J., Paulus M.P., Geyer M.A. Dopamine D4 receptor-knock-out mice exhibit reduced exploration of novel stimuli. J. Neurosci. 19:1999;9550-9556.
27. Ehringer H., Hornykiewicz O. Verteilung von Noradrenalin und Dopamin (3-Hydroxytyramin) im Gehirn des Menschen und ihr Verhalten bei Erkrankungen des extrapyrimidalen Systems. Wien. Klin. Wochenschr. 38:1960;1236-1239.
28. El Ghundi M., George S.R., Drago J., Fletcher P.J., Fan T., Nguyen T., Liu C., Sibley D.R., Westphal H., O'Dowd B.F. Disruption of dopamine D1 receptor gene expression attenuates alcohol-seeking behavior. Eur. J. Pharmacol. 353:1998;149-158.
29. El Ghundi M., Fletcher P.J., Drago J., Sibley D.R., O'Dowd B.F., George S.R. Spatial learning deficit in dopamine D(1) receptor knockout mice. Eur. J. Pharmacol. 383:1999;95-106.
30. Fauchey V., Jaber M., Caron M.G., Bloch B., Le Moine C. Differential regulation of the dopamine D1, D2 and D3 receptor gene expression and changes in the phenotype of the striatal neurons in mice lacking the dopamine transporter. Eur. J. Neurosci. 12:2000;19-26.
31. Fumagalli F., Gainetdinov R.R., Valenzano K.J., Caron M.G. Role of dopamine transporter in methamphetamine-induced neurotoxicity: evidence from mice lacking the transporter. J. Neurosci. 18:1998;4861-4869.
32. Gainetdinov R.R., Fumagalli F., Jones S.R., Caron M.G. Dopamine transporter is required for in vivo MPTP neurotoxicity: evidence from mice lacking the transporter. J. Neurochem. 69:1997;1322-1325.
33. Gainetdinov R.R., Fumagalli F., Wang Y.M., Jones S.R., Levey A.I., Miller G.W., Caron M.G. Increased MPTP neurotoxicity in vesicular monoamine transporter 2 heterozygote knockout mice. J. Neurochem. 70:1998;1973-1978.
34. George S.R., Fan T., Ng G.Y., Jung S.Y., O'Dowd B.F., Naranjo C.A. Low endogenous dopamine function in brain predisposes to high alcohol preference and consumption: reversal by increasing synaptic dopamine. J. Pharmacol. Exp. Ther. 273:1995;373-379.
35. Giros B., Jaber M., Jones S.R., Wightman R.M., Caron M.G. Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature. 379:1996;606-612.
36. Hamers F.P., Lankhorst A.J., van Laar T.J., Veldhuis W.B., Gispen W.H. Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J. Neurotrauma. 18:2001;187-201.
37. Hollon T.R., Bek M.J., Lachowicz J.E., Ariano M.A., Mezey E., Ramachandran R., Wersinger S.R., Soares-da-Silva P., Liu Z.F., Grinberg A., Drago J., Young W.S. III, Westphal H., Jose P.A., Sibley D.R. Mice lacking D5 dopamine receptors have increased sympathetic tone and are hypertensive. J. Neurosci. 22:2002;10801-10810.
38. Holmes A., Hollon T.R., Gleason T.C., Liu Z., Dreiling J., Sibley D.R., Crawley J.N. Behavioral characterization of dopamine D5 receptor null mutant mice. Behav. Neurosci. 115:2001;1129-1144.
39. Hynes M., Stone D.M., Dowd M., Pitts-Meek S., Goddard A., Gurney A., Rosenthal A. Control of cell pattern in the neural tube by the zinc finger transcription factor and oncogene Gli-1. Neuron. 19:1997;15-26.
40. Jaber M., Jones S., Giros B., Caron M.G. The dopamine transporter: a crucial component regulating dopamine transmission. Mov. Disord. 12:1997;629-633.
41. Jaber M., Dumartin B., Sagne C., Haycock J.W., Roubert C., Giros B., Bloch B., Caron M.G. Differential regulation of tyrosine hydroxylase in the basal ganglia of mice lacking the dopamine transporter. Eur. J. Neurosci. 11:1999;3499-3511.
42. Janssen P.A.J., Niemegeers C.J.E. Arzneim.-Forsch. 9:1959;765-767.
43. Jardemark K., Wadenberg M.L., Grillner P., Svensson T.H. Dopamine D3 and D4 receptor antagonists in the treatment of schizophrenia. Curr. Opin. Investig. Drugs. 3:2002;101-105.
44. Jin Y., Hoskins R., Horvitz H.R. Control of type-D GABAergic neuron differentiation by C. elegans UNC-30 homeodomain protein. Nature. 372:1994;780-783.
45. Jones S.R., Gainetdinov R.R., Jaber M., Giros B., Wightman R.M., Caron M.G. Profound neuronal plasticity in response to inactivation of the dopamine transporter. Proc. Natl. Acad. Sci. U. S. A. 95:1998;4029-4034.
46. Jones S.R., Gainetdinov R.R., Wightman R.M., Caron M.G. Mechanisms of amphetamine action revealed in mice lacking the dopamine transporter. J. Neurosci. 18:1998;1979-1986.
47. Jones S.R., Gainetdinov R.R., Hu X.T., Cooper D.C., Wightman R.M., White F.J., Caron M.G. Loss of autoreceptor functions in mice lacking the dopamine transporter. Nat. Neurosci. 2:1999;649-655.
48. Jung M.Y., Skryabin B.V., Arai M., Abbondanzo S., Fu D., Brosius J., Robakis N.K., Polites H.G., Pintar J.E., Schmauss C. Potentiation of the D2 mutant motor phenotype in mice lacking dopamine D2 and D3 receptors. Neuroscience. 91:1999;911-924.
49. Kelly M.A., Rubinstein M., Asa S.L., Zhang G., Saez C., Bunzow J.R., Allen R.G., Hnasko R., Ben Jonathan N., Grandy D.K., Low M.J. Pituitary lactotroph hyperplasia and chronic hyperprolactinemia in dopamine D2 receptor-deficient mice. Neuron. 19:1997;103-113.
50. Kelly M.A., Rubinstein M., Phillips T.J., Lessov C.N., Burkhart-Kasch S., Zhang G., Bunzow J.R., Fang Y., Gerhardt G.A., Grandy D.K., Low M.J. Locomotor activity in D2 dopamine receptor-deficient mice is determined by gene dosage, genetic background, and developmental adaptations. J. Neurosci. 18:1998;3470-3479.
51. Kim D.S., Szczypka M.S., Palmiter R.D. Dopamine-deficient mice are hypersensitive to dopamine receptor agonists. J. Neurosci. 20:2000;4405-4413.
52. Kitayama S., Shimada S., Xu H., Markham L., Donovan D.M., Uhl G.R. Dopamine transporter site-directed mutations differentially alter substrate transport and cocaine binding. Proc. Natl. Acad. Sci. U. S. A. 89:1992;7782-7785.
53. Kobayashi K., Morita S., Sawada H., Mizuguchi T., Yamada K., Nagatsu I., Hata T., Watanabe Y., Fujita K., Nagatsu T. Targeted disruption of the tyrosine hydroxylase locus results in severe catecholamine depletion and perinatal lethality in mice. J. Biol. Chem. 270:1995;27235-27243.
54. Lamonerie T., Tremblay J.J., Lanctot C., Therrien M., Gauthier Y., Drouin J. Ptx1, a bicoid-related homeo box transcription factor involved in transcription of the pro-opiomelanocortin gene. Genes Dev. 10:1996;1284-1295.
55. Law S.W., Conneely O.M., DeMayo F.J., O'Malley B.W. Identification of a new brain-specific transcription factor, NURR1. Mol. Endocrinol. 6:1992;2129-2135.
56. Lidow M.S., Goldman-Rakic P.S., Rakic P. Synchronized overproduction of neurotransmitter receptors in diverse regions of the primate cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 88:1991;10218-10221.
57. Liu H., Brown J.L., Jasmin L., Maggio J.E., Vigna S.R., Mantyh P.W., Basbaum A.I. Synaptic relationship between substance P and the substance P receptor: light and electron microscopic characterization of the mismatch between neuropeptides and their receptors. Proc. Natl. Acad. Sci. U. S. A. 91:1994;1009-1013.
58. Malmberg A., Jackson D.M., Eriksson A., Mohell N. Unique binding characteristics of antipsychotic agents interacting with human dopamine D2A, D2B, and D3 receptors. Mol. Pharmacol. 43:1993;749-754.
59. Martinez S., Crossley P.H., Cobos I., Rubenstein J.L., Martin G.R. FGF8 induces formation of an ectopic isthmic organizer and isthmocerebellar development via a repressive effect on Otx2 expression. Development. 126:1999;1189-1200.
60. Matsuo I., Kuratani S., Kimura C., Takeda N., Aizawa S. Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 9:1995;2646-2658.
61. Meltzer H.Y., Stahl S.M. The dopamine hypothesis of schizophrenia: a review. Schizophr. Bull. 2:1976;19-76.
62. Millet S., Campbell K., Epstein D.J., Losos K., Harris E., Joyner A.L. A role for Gbx2 in repression of Otx2 and positioning the mid/hindbrain organizer. Nature. 401:1999;161-164.
63. Ng G.Y., George S.R. Dopamine receptor agonist reduces ethanol self-administration in the ethanol-preferring C57BL/6J inbred mouse. Eur. J. Pharmacol. 269:1994;365-374.
64. Nishii K., Matsushita N., Sawada H., Sano H., Noda Y., Mamiya T., Nabeshima T., Nagatsu I., Hata T., Kiuchi K., Yoshizato H., Nakashima K., Nagatsu T., Kobayashi K. Motor and learning dysfunction during postnatal development in mice defective in dopamine neuronal transmission. J. Neurosci. Res. 54:1998;450-464.
65. Rhinn M., Dierich A., Shawlot W., Behringer R.R., Le Meur M., Ang S.L. Sequential roles for Otx2 in visceral endoderm and neuroectoderm for forebrain and midbrain induction and specification. Development. 125:1998;845-856.
66. Rios M., Habecker B., Sasaoka T., Eisenhofer G., Tian H., Landis S., Chikaraishi D., Roffler-Tarlov S. Catecholamine synthesis is mediated by tyrosinase in the absence of tyrosine hydroxylase. J. Neurosci. 19:1999;3519-3526.
67. Rubinstein M., Phillips T.J., Bunzow J.R., Falzone T.L., Dziewczapolski G., Zhang G., Fang Y., Larson J.L., McDougall J.A., Chester J.A., Saez C., Pugsley T.A., Gershanik O., Low M.J., Grandy D.K. Mice lacking dopamine D4 receptors are supersensitive to ethanol, cocaine, and methamphetamine. Cell. 90:1997;991-1001.
68. Sakurada K., Ohshima-Sakurada M., Palmer T.D., Gage F.H. Nurr1, an orphan nuclear receptor, is a transcriptional activator of endogenous tyrosine hydroxylase in neural progenitor cells derived from the adult brain. Development. 126:1999;4017-4026.
69. Saucedo-Cardenas O., Quintana-Hau J.D., Le W.D., Smidt M.P., Cox J.J., De Mayo F., Burbach J.P., Conneely O.M. Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc. Natl. Acad. Sci. U. S. A. 95:1998;4013-4018.
70. Seeman P. Dopamine receptor sequences. Therapeutic levels of neuroleptics occupy D2 receptors, clozapine occupies D4. Neuropsychopharmacology. 7:1992;261-284.
71. Semina E.V., Reiter R., Leysens N.J., Alward W.L., Small K.W., Datson N.A., Siegel-Bartelt J., Bierke-Nelson D., Bitoun P., Zabel B.U., Carey J.C., Murray J.C. Cloning and characterization of a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome. Nat. Genet. 14:1996;392-399.
72. Semina E.V., Reiter R.S., Murray J.C. Isolation of a new homeobox gene belonging to the Pitx/Rieg family: expression during lens development and mapping to the aphakia region on mouse chromosome 19. Hum. Mol. Genet. 6:1997;2109-2116.
73. Semina E.V., Ferrell R.E., Mintz-Hittner H.A., Bitoun P., Alward W.L., Reiter R.S., Funkhauser C., Daack-Hirsch S., Murray J.C. A novel homeobox gene PITX3 is mutated in families with autosomal-dominant cataracts and ASMD. Nat. Genet. 19:1998;167-170.
74. Simeone A., D'Apice M.R., Nigro V., Casanova J., Graziani F., Acampora D., Avantaggiato V. Orthopedia, a novel homeobox-containing gene expressed in the developing CNS of both mouse and Drosophila. Neuron. 13:1994;83-101.
75. Simon H.H., Saueressig H., Wurst W., Goulding M.D., O'Leary D.D. Fate of midbrain dopaminergic neurons controlled by the engrailed genes. J. Neurosci. 21:2001;3126-3134.
76. Smidt M.P., van Schaick H.S., Lanctot C., Tremblay J.J., Cox J.J., van der Kleij A.A., Wolterink G., Drouin J., Burbach J.P. A homeodomain gene Ptx3 has highly restricted brain expression in mesencephalic dopaminergic neurons. Proc. Natl. Acad. Sci. U. S. A. 94:1997;13305-13310.
77. Spielewoy C., Gonon F., Roubert C., Fauchey V., Jaber M., Caron M.G., Roques B.P., Hamon M., Betancur C., Maldonado R., Giros B. Increased rewarding properties of morphine in dopamine-transporter knockout mice. Eur. J. Neurosci. 12:2000;1827-1837.
78. Starr M.S. Glutamate/dopamine D1/D2 balance in the basal ganglia and its relevance to Parkinson's disease. Synapse. 19:1995;264-293.
79. Steiner H., Fuchs S., Accili D. D3 dopamine receptor-deficient mouse: evidence for reduced anxiety. Physiol. Behav. 63:1997;137-141.
80. Takahashi N., Miner L.L., Sora I., Ujike H., Revay R.S., Kostic V., Jackson-Lewis V., Przedborski S., Uhl G.R. VMAT2 knockout mice: heterozygotes display reduced amphetamine-conditioned reward, enhanced amphetamine locomotion, and enhanced MPTP toxicity. Proc. Natl. Acad. Sci. U. S. A. 94:1997;9938-9943.
81. Ungerstedt U., Ljungberg T., Steg G. Behavioral, physiological, and neurochemical changes after 6-hydroxydopamine-induced degeneration of the nigro-striatal dopamine neurons. Adv. Neurol. 5:1974;421-426.
82. Van den Munckhof P., Luk K.C., Ste-Marie L., Montgomery J., Blanchet P.J., Sadikot A.F., Drouin J. Pitx3 is required for motor activity and for survival of a subset of midbrain dopaminergic neurons. Development. 130:2003;2535-2542.
83. Von Euler U., Lishajko F. Dopamine in mammalian lung and spleen. Acta Physiol. Pharmacol. Neerl. 6:1957;295-303.
84. Vorbruggen G., Constien R., Zilian O., Wimmer E.A., Dowe G., Taubert H., Noll M., Jackle H. Embryonic expression and characterization of a Ptx1 homolog in Drosophila. Mech. Dev. 68:1997;139-147.
85. Wagner A.F., Cirillo V.J., Meisinger M.A., Ormond R.E., Kuehl F.A. Jr., Brink N.G. A further study of catecholamine omicron-methylation in schizophrenia. Nature. 211:1966;604-605.
86. Wang Y.M., Gainetdinov R.R., Fumagalli F., Xu F., Jones S.R., Bock C.B., Miller G.W., Wightman R.M., Caron M.G. Knockout of the vesicular monoamine transporter 2 gene results in neonatal death and supersensitivity to cocaine and amphetamine. Neuron. 19:1997;1285-1296.
87. Wassef M., Joyner A.L. Early mesencephalon/metencephalon patterning and development of the cerebellum. Perspect. Dev. Neurobiol. 5:1997;3-16.
88. Wurst W., Auerbach A.B., Joyner A.L. Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development. 120:1994;2065-2075.
89. Xu M., Moratalla R., Gold L.H., Hiroi N., Koob G.F., Graybiel A.M., Tonegawa S. Dopamine D1 receptor mutant mice are deficient in striatal expression of dynorphin and in dopamine-mediated behavioral responses. Cell. 79:1994;729-742.
90. Xu M., Koeltzow T.E., Santiago G.T., Moratalla R., Cooper D.C., Hu X.T., White N.M., Graybiel A.M., White F.J., Tonegawa S. Dopamine D3 receptor mutant mice exhibit increased behavioral sensitivity to concurrent stimulation of D1 and D2 receptors. Neuron. 19:1997;837-848.
91. Xu Y., Stokes A.H., Freeman W.M., Kumer S.C., Vogt B.A., Vrana K.E. Tyrosinase mRNA is expressed in human substantia nigra. Brain Res. Mol. Brain Res. 45:1997;159-162.
92. Ye W., Shimamura K., Rubenstein J.L., Hynes M.A., Rosenthal A. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell. 93:1998;755-766.
93. Yu Y., Li W., Su K., Yussa M., Han W., Perrimon N., Pick L. The nuclear hormone receptor Ftz-F1 is a cofactor for the Drosophila homeodomain protein Ftz. Nature. 385:1997;552-555.
94. Zetterström R.H., Solomin L., Jansson L., Hoffer B.J., Olson L., Perlmann T. Dopamine neuron agenesis in Nurr1-deficient mice. Science. 276:1997;248-250.
95. Zhou Q.Y., Palmiter R.D. Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell. 83:1995;1197-1209.
96. Zhou Q.Y., Quaife C.J., Palmitter R.D. Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature. 374:1995;640-643.