Cell type-specific gene expression of midbrain dopaminergic neurons reveals molecules involved in their vulnerability and protection

Human Molecular Genetics

Volumn 14, Issue 13, 2005, Pages 1709-1725

  Chung, Chee Yeun ^a,b   Seo, Hyemyung ^a,d   Sonntag, Kai Christian ^a   Brooks, Andrew ^c   Lin, Ling ^a   Isacson, Ole ^a,b  

^a MCLEAN HOSPITAL   (United States)

^b The Harvard Center for Neurodegeneration & Repair   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^d Hanyang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ALPHA SYNUCLEIN; AQUAPORIN 4; CALBINDIN; CALCITONIN GENE RELATED PEPTIDE; CHOLECYSTOKININ; COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; EARLY GROWTH RESPONSE FACTOR 1; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 3; GAMMA SYNUCLEIN; GAP JUNCTION PROTEIN; GASTRIN RELEASING PEPTIDE; GLUCOSE REGULATED PROTEIN; GROWTH HORMONE RECEPTOR; HERMES ANTIGEN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; INWARDLY RECTIFYING POTASSIUM CHANNEL; LIPOPROTEIN LIPASE; MARCKS PROTEIN; NEUROPILIN 2; PHOSPHOPROTEIN; PROTIRELIN RECEPTOR; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN C; SORCIN; TYROSINASE RELATED PROTEIN 1; VASOACTIVE INTESTINAL POLYPEPTIDE; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; CELL STRAIN; CELL TYPE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DNA MICROARRAY; DOPAMINERGIC NERVE CELL; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; LASER CAPTURE MICRODISSECTION; MESENCEPHALON; MOUSE; NERVE CELL CULTURE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; UNINDEXED SEQUENCE; VALIDATION PROCESS;

1-METHYL-4-PHENYLPYRIDINIUM; ANIMALS; DOPAMINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HERBICIDES; MESENCEPHALON; MICE; MPTP POISONING; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARKINSON DISEASE; PC12 CELLS; RATS;

FORMICIDAE;

EID: 26444529541     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddi178     Document Type: Article

References (91)

1. McRitchie, D.A., Hardman, C.D. and Halliday, G.M. (1996) Cytoarchitectural distribution of calcium binding proteins in midbrain dopaminergic regions of rats and humans. J. Comp. Neurol., 364 121-150.
2. Neuhoff, H., Neu, A., Liss, B. and Roeper, J. (2002) I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J. Neurosci., 22 1290-1302.
3. Wolfart, J., Neuhoff, H., Franz, O. and Roeper, J. (2001) Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J. Neurosci., 21, 3443-3456.
4. Gorell, J.M., Peterson, E.L., Rybicki, B.A. and Johnson. C.C. (2004) Multiple risk factors for Parkinson's disease. J. Neurol. Sci., 217, 169-174.
5. Tanner, C.M., Ottman, R., Goldman, S.M., Ellenberg, J., Chan, P., Mayeux, R. and Langston, J.W. (1999) Parkinson disease in twins: An etiologic study. JAMA, 281, 341-346.
6. Polymeropoulos, M.H., Lavedan, C., Leroy, E., Ide, S.E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R. et al. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science, 276, 2045-2047.
7. Leroy, E., Boyer, R., Auburger, G., Leube, B., Ulm, G., Mezey, E., Harta. G., Brownstein, M.J., Jonnalagada, S., Chernova, T. et al. (1998) The ubiquitin pathway in Parkinson's disease. Nature, 395, 451-452.
8. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y. and Shimizu, N. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature, 392, 605-608.
9. Bonifati, V., Rizzu, P., van Baren, M.J., Schaap, O., Breedveld, G.J., Krieger, E., Dekker, M.C., Squitieri, F., Ibanez, P., Joosse, M. et al. (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science, 299, 256-259.
10. Valente, E.M., Abou-Sleiman, P.M., Caputo, V., Muqit, M.M., Harvey, K., Gispert, S., Ali, Z., Del Turco, D., Bentivoglio, A.R., Healy, D.G. et al. (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science, 304, 1158-1160.
11. Singleton, A.B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum. R. et al. (2003) alpha-Synuclein locus triplication causes Parkinson's disease. Science, 302, 841.
12. Hirsch, E., Graybiel, A.M. and Agid, Y.A. (1988) Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature, 334, 345-348.
13. German, D.C., Manaye, K.F., Sonsalla, P.K. and Brooks, B.A. (1992) Midbrain dopaminergic cell loss in Parkinson's disease and MPTP-induced parkinsonism: Sparing of calbindin-D28k-containing cells. Ann. N Y Acad. Sci., 648, 42-62.
14. Damier, P., Hirsch. E.C., Agid, Y. and Graybiel, A.M. (1999) The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain, 122 1437-1448.
15. German, D.C., Manaye, K., Smith, W.K., Woodward, D.J. and Saper, C.B. (1989) Midbrain dopaminergic cell loss in Parkinson's disease: Computer visualization. Ann. Neurol., 26, 507-514.
16. German, D.C., Dubach, M., Askari, S., Speciale, S.G. and Bowden, D.M. (1988) 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonian syndrome in Macaca fascicularis: Which midbrain dopaminergic neurons are lost? Neuroscience, 24, 161-174.
17. Rodriguez, M., Barroso-Chinea, P., Abdala, P., Obeso, J. and Gonzalez-Hernandez, T. (2001) Dopamine cell degeneration induced by intraventricular administration of 6-hydroxydopamine in the rat: similarities with cell loss in parkinson's disease. Exp. Neurol., 169, 163-181.
18. Pakkenberg, B., Moller, A., Gundersen, H.J., Mouritzen Dam, A. and 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. J. Neurol. Neurosurg. Psychiatry, 54, 30-33.
19. McGeer, P.L., Itagaki, S., Akiyama, H. and McGeer, E.G. (1988) Rate of cell death in parkinsonism indicates active neuropathological process. Ann. Neurol., 24, 574-576.
20. Fearnley, J.M. and Lees, A.J. (1991) Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain, 114, 2283-2301.
21. Javoy-Agid, F. and Agid, Y. (1980) Is the mesocortical dopaminergic system involved in Parkinson disease? Neurology, 30, 1326-1330.
22. McRitchie, D.A., Cartwright, H.R. and Halliday, G.M. (1997) Specific A10 dopaminergic nuclei in the midbrain degenerate in Parkinson's disease. Exp. Neurol., 144, 202-213.
23. Yamada, T., McGeer, P.L., Baimbridge, K.G. and McGeer, E.G. (1990) Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28K. Brain Res., 526, 303-307.
24. Parent, A., Fortin, M., Cote, P.Y. and Cicchetti, F. (1996) Calcium-binding proteins in primate basal ganglia. Neurosci. Res., 25, 309-334.
25. Liang, C.L., Sinton, C.M., Sonsalla, P.K. and German, D.C. (1996) Midbrain dopaminergic neurons in the mouse that contain calbindin-D28k exhibit reduced vulnerability to MPTP-induced neurodegeneration, Neurodegeneration, 5, 313-318.
26. Schein, J.C., Hunter, D.D. and Roper-Tarlov, S. (1998) Girk2 expression in the ventral midbrain, cerebellum, and olfactory bulb and its relationship to the murine mutation weaver. Dev. Biol., 204, 432-450.
27. + channel mRNAs are differentially expressed in the adult rat brain. J. Neurosci., 16, 3559-3570.
28. Roffler-Tarlov, S., Martin, B., Graybiel, A.M. and Kauer, J.S. (1996) Cell death in the midbrain of the murine mutation weaver. J. Neurosci., 16, 1819-1826.
29. Liss, B., Neu, A. and Roeper, J. (1999) The weaver mouse gain-of-function phenotype of dopaminergic midbrain neurons is determined by coactivation of wvGirk2 and K-ATP channels. J. Neurosci., 19, 8839-8848.
30. + channels composed of Kir3.2 subunits in dopaminergic neurons of the substantia nigra. J. Neurosci., 19, 1006-1017.
31. Isacson, O. (1993) On neuronal health. Trends Neurosci., 16, 306-308.
32. Seo, H., Sonntag, K.C. and Isacson, O. (2004) Generalized brain and skin proteasome inhibition in Huntington's disease. Ann. Neurol., 56 319-328.
33. McCaffery, P. and Drager, U.C. (1994) High levels of a retinoic acid-generating dehydrogenase in the mesa-telencephalic dopamine system. Proc. Natl Acad. Sci. USA, 91, 7772-7776.
34. Sirinathsinghji, D.J., Kupsch, A., Mayer, E., Zivin, M., Pufal, D. and Oertel, W.H. (1992) Cellular localization of tyrosine hydroxylase mRNA and cholecystokinin mRNA-containing cells in the ventral mesencephalon of the common marmoset: Effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Brain Res. Mol. Brain Res. 12, 267-274.
35. Seroogy, K.B., Dangaran, K., Lim, S., Haycock, J.W. and Fallon, J.H. (1989) Ventral mesencephalic neurons containing both cholecystokinin-and tyrosine hydroxylase-like immunoreactivities project to forebrain regions. J. Comp. Neurol., 279, 397-414.
36. Draghici, S., Khatri, P., Martins, R.P., Ostermeier, G.C. and Krawetz, S.A. (2003) Global functional profiling of gene expression. Genomics 81, 98-104.
37. Seabra, M.C., Mules, E.H. and Hume, A.N. (2002) Rab GTPases, intracellular traffic and disease. Trends Mol. Med., 8, 23-30.
38. O'Connor, L., Strasser, A., O'Reilly, L.A., Hausmann, G., Adams, J.M., Cory, S. and Huang, D.C. (1998) Bim: A novel member of the Bcl-2 family that promotes apoptosis. EMBO J., 17, 384-395.
39. Tanaka, Y., Engelender, S., Igarashi, S., Rao, R.K., Wanner, T., Tanzi, R.E., Sawa, A., V, L.D.. Dawson, T.M. and Ross, C.A. (2001) Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis. Hum. Mol. Genet., 10, 919-926.
40. Przedborski, S., Tieu, K., Perier, C. and Vila, M. (2004) MPTP as a mitochondrial neurotoxic model of Parkinson's disease. J. Bioenerg. Biomembr., 36, 375-379.
41. Bayer, S.A., Triarhou, L.C., Thomas, J.D. and Ghetti, B. (1994) Correlated quantitative studies of the neostriatum, nucleus accumbens, substantia nigra, and ventral tegmental area in normal and weaver mutant mice. J. Neurosci., 14, 6901-6910.
42. Graybiel, A.M., Ohta, K. and Roffter-Tarlov, S. (1990) Patterns of cell and fiber vulnerability in the mesostriatal system of the mutant mouse weaver. I. Gradients and compartments. J. Neurosci., 10, 720-733.
43. Halestrap, A.P. and Brennerb, C. (2003) The adenine nucleotide translocase: A central component of the mitochondrial permeability transition pore and key player in cell death. Curr. Med. Chem., 10, 1507-1525.
44. Marzo, I., Brenner, C., Zamzami, N., Jurgensmeier, J.M., Susin, S.A., Vieira, H.L., Prevost, M.C., Xie, Z., Matsuyama, S., Reed, J.C. et al. (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science, 281, 2027-2031.
45. Lu, T., Pan, Y., Kao, S.Y., Li, C., Kohane, I., Chan, J. and Yankner, B.A. (2004) Gene regulation and DNA damage in the ageing human brain. Nature, 429, 883-891
46. Quesada, A. and Micevych, P.E. (2004) Estrogen interacts with the IGF-1 system to protect nigrostriatal dopamine and maintain motoric behavior after 6-hydroxdopamine lesions. J. Neurosci. Res., 75, 107-116.
47. Krishnamurthi, R., Stott, S., Maingay, M., Faull, R.L., McCarthy, D., Gluckman, P. and Guan, J. (2004) N-terminal tripeptide of IGF-1 improves functional deficits after 6-OHDA lesion in rats. Neuroreport, 15, 1601-1604.
48. Wickman, K. and Clapham, D.E. (1995) Ion channel regulation by G proteins. Physiol. Rev., 75, 865-885.
49. + channels. Neuron, 16, 321-331.
50. Palmieri, F. (2004) The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch., 447, 689-709.
51. Cassarino, D.S., Parks, J. K., Parker, W.D., Jr. and Bennett, J.P., Jr. (1999) The parkinsonian neurotoxin MPP+ opens the mitochondrial permeability transition pore and releases cytochrome c in isolated mitochondria via an oxidative mechanism. Biochim. Biophys. Acta, 1453, 49-62.
52. Kiranadi, B., Bangham, J.A. and Smith, P.A. (1991) Inhibition of electrical activity in mouse pancreatic beta-cells by the ATP/ADP translocase inhibitor, bongkrekic acid. FEBS Lett., 283, 93-96.
53. Guan, J., Miller, O.T., Waugh, K.M., McCarthy, D.C. and Gluckman, P.D. (2001) Insulin-like growth factor-1 improves somatosensory function and reduces the extent of cortical infarction and ongoing neuronal loss after hypoxia-ischemia in rats. Neuroscience, 105, 299-306.
54. Wang, J.M., Hayashi, T., Zhang, W.R., Sakai, K., Shiro, Y. and Abe, K. (2000) Reduction of ischemic brain injury by topical application of insulin-like growth factor-I after transient middle cerebral artery occlusion in rats. Brain Res., 859, 381-385.
55. Kermer, P., Klocker, N., Labes, M. and Bahr, M. (2000) Insulin-like growth factor-I protects axotomized rat retinal ganglion cells from secondary death via P13-K-dependent Akt phosphorylation and inhibition of caspase-3 in vivo. J Neurosci., 20, 2-8.
56. Poe, B.H.. Linville, C., Riddle, D.R., Sonntag, W.E. and Brunso-Bechtold, J.K. (2001) Effects of age and insulin-like growth factor-1 on neuron and synapse numbers in area CA3 of hippocampus. Neuroscience, 107, 231-238.
57. Vincent, A.M., Mobley, B.C., Hiller, A. and Feldman, E.L. (2004) IGF-I prevents glutamate-induced motor neuron programmed cell death. Neurobiol. Dis., 16, 407-416.
58. Zawada, W.M., Kirschman, D.L., Cohen, J.J., Heidenreich, K.A. and Freed, C.R. (1996) Growth factors rescue embryonic dopamine neurons from programmed cell death. Exp. Neurol., 140, 60-67.
59. Shavali, S., Ren, J. and Ebadi, M. (2003) Insulin-like growth factor-1 protects human dopaminergic SH-SY5Y cells from salsolinol-induced toxicity. Neurosci. Lett., 340, 79-82.
60. Strasburger, C.J., Bidlingmaier, M., Wu, Z. and Morrison, K.M. (2001) Normal values of insulin-like growth factor I and their clinical utility in adults. Horm. Res., 55(Suppl. 2), 100-105.
61. van Dam, P.S. and Aleman, A. (2004) Insulin-like growth factor-I, cognition and brain aging. Eur. J. Pharmacol., 490, 87-95.
62. Yegen, B.C. (2003) Bombesin-like peptides: Candidates as diagnostic and therapeutic tools. Curr. Pharm. Des., 9, 1013-1022.
63. Cuttitta, F., Carney, D.N., Mulshine, J., Moody, T.W., Fedorko, J., Fischler, A. and Minna, J.D. (1985) Bombesin-like peptides can function as autocrine growth factors in human small-cell lung cancer. Nature 316, 823-826.
64. Alexander, R.W., Upp, J.R., Jr., Poston, G.J., Gupta, V., Townsend, C.M., Jr. and Thompson, J.C. (1988) Effects of bombesin on growth of human small cell lung carcinoma in vivo. Cancer Res., 48, 1439-1441.
65. Larsen, P.J., Saermark, T. and Mikkelsen, J.D. (1989) An immunohistochemical demonstration of gastrin-releasing peptide (GRP) in the rat substantia nigra. J. Chem. Neuroanat, 2, 83-93.
66. Goodman, E.C. and Iversen, L.L. (1986) Calcitonin gene-related peptide: novel neuropeptide. Life Sci., 38, 2169-2178.
67. Bell, D. and McDermott, B.J. (1996) Calcitonin gene-related peptide in the cardiovascular system: Characterization of receptor populations and their (patho)physiological significance. Pharmacol. Rev., 48 253-288.
68. Burvenich, S., Unsicker, K. and Krieglstein, K. (1998) Calcitonin gene-related peptide promotes differentiation, but not survival, of rat mesencephalic dopaminergic neurons in vitro. Neuroscience, 86 1165-1172.
69. Arimura, A. (1992) Pituitary adenylate cyclase activating polypeptide (PACAP): Discovery and current status of research. Regul. Pept., 37, 287-303.
70. Ogi, K., Kimura, C., Onda, H., Arimura, A. and Fujino, M. (1990) Molecular cloning and characterization of cDNA for the precursor of rat pituitary adenylate cyclase activating polypeptide (PACAP). Biochem. Biophys. Res. Commun., 173, 1271-1279.
71. Vaudry, D., Gonzalez, B.J., Basille, M., Yon. L., Fournier, A. and Vaudry, H. (2000) Pituitary adenylate cyclase-activating polypeptide and its receptors: From structure to functions. Pharmacol. Rev., 52 269-324.
72. Arimura, A. (1998) Perspectives on pituitary adenylate cyclase activating polypeptide (PACAP) in the neuroendocrine, endocrine, and nervous systems. Jpn. J. Physiol., 48, 301-331.
73. Reglodi, D., Lubics, A., Tamas, A., Szalontay, L. and Lengvari, I. (2004) Pituitary adenylate cyclase activating polypeptide protects dopaminergic neurons and improves behavioral deficits in a rat model of Parkinson's disease. Behav Brain. Res., 151, 303-312.
74. Takei, N., Skoglosa, Y. and Lindholm, D. (1998) Neurotrophic and neuroprotective effects of pituitary adenylate cyclase-activating polypeptide (PACAP) on mesencephalic dopaminergic neurons. J. Neurosci. Res., 54, 698-706.
75. Delgado, M. and Ganea, D. (2003) Neuroprotective effect of vasoactive intestinal peptide (VIP) in a mouse model of Parkinson's disease by blocking microglial activation. FASEB J., 17, 944-946.
76. Dogrukol-Ak, D., Tore, F. and Tuncel, N. (2004) Passage of VIP/PACAP/ secretin family across the blood-brain barrier: Therapeutic effects. Curr. Pharm. Des., 10, 1325-1340.
77. Greenamyre, J.T., Sherer, T.B., Betarbet, R. and Panov, A.V. (2001) Complex I and Parkinson's disease. IUBMB Life, 52, 135-141.
78. Betarbet, R., Sherer, T.B., MacKenzie, G., Garcia-Osuna, M., Panov, A.V. and Greenamyre, J.T. (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci., 3 1301-1306.
79. Beal, M.F. (2004) Commentary on 'alpha-synuclein and mitochondria: A tangled skein'. Exp. Neurol., 186, 109-111.
80. Hsu, L.J., Sagara, Y., Arroyo. A., Rockenstein, E., Sisk, A., Mallory, M., Wong, J., Takenouchi, T., Hashimoto, M. and Masliah, E. (2000) alpha-synuclein promotes mitochondrial deficit and oxidative stress. Am. J. Pathol., 157, 401-410.
81. Palacino, J.J., Sagi, D., Goldberg, M.S., Krauss, S., Motz, C., Wacker, M., Klose, J. and Shen, J. (2004) Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. J. Biol. Chem., 279 18614-18622.
82. Graham, D.G. (1978) Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol. Pharmacol., 14, 633-643.
83. Ciliax, B.J., Drash, G.W., Staley, J.K., Haber, S., Mobley, C.J., Miller, G.W., Mufson, E.J., Mash, D.C. and Levey, A.I. (1999) Immunocytochemical localization of the dopamine transporter in human brain. J. Comp. Neurol., 409, 38-56.
84. Haber, S.N., Ryoo, H., Cox, C. and Lu, W. (1995) Subsets of midbrain dopaminergic neurons in monkeys are distinguished by different levels of mRNA for the dopamine transporter: Comparison with the mRNA for the D2 receptor, tyrosine hydroxylase and calbindin immunoreactivity. J. Comp. Neurol., 362, 400-410.
85. Uhl, G.R., Walther, D., Mash, D., Faucheux, B. and Javoy-Agid, F. (1994) Dopamine transporter messenger RNA in Parkinson's disease and control substantia nigra neurons. Ann. Neurol., 35, 494-498.
86. Aubert, I., Brana, C., Pellevoisin, C., Giros, B., Caille, I., Carles, D., Vital, C. and Bloch, B. (1997) Molecular anatomy of the development of the human substantia nigra. J. Comp. Neurol., 379, 72-87.
87. Willingham, S., Outeiro, T.F., DeVit, M.J., Lindquist, S.L. and Muchowski, P.J. (2003) Yeast genes that enhance the toxicity of a mutant huntington fragment or alpha-synuclein. Science, 302, 1769-1772.
88. Hauser, M.A., Li, Y.J., Takeuchi, S., Walters, R., Noureddine, M., Maready, M., Darden, T., Hulette, C., Martin, E., Hauser, E. et al. (2003) Genomic convergence: Identifying candidate genes for Parkinson's disease by combining serial analysis of gene expression and genetic linkage. Hum. Mol. Genet., 12, 671-677.
89. Grimm, J., Mueller, A., Hefti, F. and Rosenthal, A. (2004) Molecular basis for catecholaminergic neuron diversity. Proc. Natl Acad. Sci. USA, 101, 13891-13896.
90. Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 25, 402-408.
91. Zufferey, R., Dull, T., Mandel, R.J., Bukovsky, A., Quiroz, D., Naldini, L. and Trono, D. (1998) Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J. Virol., 72, 9873-9880.