Moving beyond tyrosine hydroxylase to define dopaminergic neurons for use in cell replacement therapies for Parkinson's disease

CNS and Neurological Disorders - Drug Targets

Volumn 11, Issue 4, 2012, Pages 340-349

  White, Robert B ^a,b   Thomas, Meghan G ^a,b  

^a EDITH COWAN UNIVERSITY   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Cell replacement therapy; Dopaminergic neuron; Nurr1; Parkinson's disease; Pitx3; Transcriptional regulation; Tyrosine hydroxylase

Indexed keywords

ADRENALIN; AZACITIDINE; BUTYRIC ACID; DOPAMINE; DOPAMINE TRANSPORTER; GROWTH FACTOR; HALOPERIDOL; HEPATOCYTE NUCLEAR FACTOR 3BETA; LEVODOPA; NEUROTRANSMITTER; NICOTINE; NORADRENALIN; NUCLEAR RECEPTOR RELATED FACTOR 1; RESERPINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PITX3; TYROSINE 3 MONOOXYGENASE;

CELL BASED GENE THERAPY; CELL DENSITY; CELL DIFFERENTIATION; CELL REPLACEMENT THERAPY; CELL SELECTION; CELL THERAPY; CHROMATIN; CHROMATIN REMODELLING; CLINICAL FEATURE; CPG ISLAND; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; ENZYME ACTIVATION; ENZYME INHIBITION; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; INFANT DISEASE; INFANTILE PARKINSONISM; INTRON; MESENCEPHALON; MOTOR DYSFUNCTION; NERVE CELL DIFFERENTIATION; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PATHOLOGY; PROMOTER REGION; PROTEIN EXPRESSION; REVIEW; TRANSCRIPTION REGULATION;

EID: 84862562553     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/187152712800792758     Document Type: Review

References (76)

1. Isacson, O. The production and use of cells as therapeutic agents in neurodegenerative diseases. Lancet Neurol., 2003, 2(7), 417-424.
2. Elsworth, J.D.; Roth, R.H. Dopamine synthesis, uptake, metabolism, and receptors: relevance to gene therapy of Parkinson's disease. Exp. Neurol., 1997, 144(1), 4-9.
3. Alder, C.H. Nonmotor complications in Parkinson's disease. Mov. Disord., 2005, (Suppl 11), S23-S29.
4. Vernier, P.; Moret, F.; Callier, S.; Snapyan, M.; Wersinger, C.; Sidhu, A. The degeneration of dopamine neurons in Parkinson's disease: insights from embryology and evolution of the mesostriatocortical system. Ann. NY Acad. Sci., 2004, 1035, 231-249.
5. Marsden, C.D. Problems with long-term levodopa therapy for Parkinson's disease. Clin. Neuropharmacol., 1994, 17(Suppl 2), S32-S44.
6. Kempster, P.A.; Williams, D.R.; Selikhova, M.; Holton, J.; Revesz, T.; Lees, A.J. Patterns of levodopa response in Parkinson's disease: a clinico-pathological study. Brain, 2007, 130(8), 2123-2128.
7. Dahlstrom, A.; Fuxe, K. Localization of monoamines in the lower brain stem. Experientia, 1964, 20(7), 398-399.
8. Wallen, A.; Perlmann, T. Transcriptional control of dopamine neuron development. Ann. NY Acad. Sci., 2003, 991, 48-60.
9. Thompson, L.; Barraud, P.; Andersson, E.; Kirik, D.; Bjorklund, A. Identification of dopaminergic neurons of nigral and ventral tegmental area subtypes in grafts of fetal ventral mesencephalon based on cell morphology, protein expression, and efferent projections. J. Neurosci., 2005, 25(27), 6467-6477.
10. Thomas, M.G. Parkinson's Disease: A study of the role of transcription factors in cell therapies. Regen. Med., 2010, 5(3), 441-450.
11. Furukawa, Y. Genetics and biochemistry of dopa-responsive dystonia: significance of striatal tyrosine hydroxylase protein loss. Adv. Neurol., 2003, 91, 401-410.
12. Hoffmann, G.F.; Assmann, B.; Brautigam, C.; Dionisi-Vici, C.; Haussler, M.; de Klerk, J.B.; Naumann, M.; Steenbergen-Spanjers, G.C.; Strassburg, H.M.; Wevers, R.A. Tyrosine hydroxylase deficiency causes progressive encephalopathy and dopanonresponsive dystonia. Ann. Neurol., 2003, 5 (Suppl 6), S56-S65.
13. Giovanniello, T.; Claps, D.; Carducci, C.; Blau, N.; Vigevano, F.; Antonozzi, I.; Leuzzi, V. A new tyrosine hydroxylase genotype associated with early-onset severe encephalopathy. J. Child. Neurol., 2011, 27(4), 523-525.
14. Daubner, S.C.; Le, T.; Wang, S. Tyrosine hydroxylase and regulation of dopamine synthesis. Arch. Biochem. Biophys., 2011, 508(1), 1-12.
15. Kobayashi, K.; Nagatsu, T. Molecular genetics of tyrosine 3-monooxygenase and inherited diseases. Biochem. Biophys. Res. Commun., 2005, 338(1), 267-270.
16. Eells, J.B. The control of dopamine neuron development, function and survival: insights from transgenic mice and the relevance to human disease. Curr. Med. Chem., 2003, 10(10), 857-870.
17. Thomas, S.A.; Matsumoto, A.M.; Palmiter, R.D. Noradrenaline is essential for mouse fetal development. Nature, 1995, 374(6523), 643-646.
18. Gates, M.A.; Torres, E.M.; White, A.; Fricker-Gates, R.A.; Dunnett, S.B. Re-examining the ontogeny of substantia nigra dopamine neurons. Eur. J. Neurosci., 2006, 23(5), 1384-1390.
19. Matsushita, N.; Okada, H.; Yasoshima, Y.; Takahashi, K.; Kiuchi, K.; Kobayashi, K. Dynamics of tyrosine hydroxylase promoter activity during midbrain dopaminergic neuron development. J. Neurochem., 2002, 82(2), 295-304.
20. Smidt, M.P.; Burbach, J.P. Terminal differentiation ofmesodiencephalic dopaminergic neurons: the role of Nurr1 and Pitx3. Adv. Exp. Med. Biol., 2009, 651, 47-57.
21. Yan, Y.; Yang, D.; Zarnowska, E.D.; Du, Z.; Werbel, B.; Valliere, C.; Pearce, R.A.; Thomson, J.A.; Zhang, S.C. Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells, 2005, 23(6), 781-790.
22. Chiba, S.; Lee, Y.M.; Zhou, W.; Freed, C.R. Noggin enhances dopamine neuron production from human embryonic stem cells and improves behavioral outcome after transplantation into Parkinsonian rats. Stem Cells, 2008, 26(11), 2810-2820.
23. Kessler, M.A.; Yang, M.; Gollomp, K.L.; Jin, H.; Iacovitti, L. The human tyrosine hydroxylase gene promoter. Brain Res. Mol. Brain Res., 2003, 112(1-2), 8-23.
24. Zhou, W.; Lee, Y.M.; Guy, V.C.; Freed, C.R. Embryonic stem cells with GFP knocked into the dopamine transporter yield purified dopamine neurons in vitro and from knock-in mice. Stem Cells, 2009, 27(12), 2952-2961.
25. Xiao, H.; Hirata, Y.; Isobe, K.; Kiuchi, K. Glial cell line-derived neurotrophic factor up-regulates the expression of tyrosine hydroxylase gene in human neuroblastoma cell lines. J. Neurochem., 2002, 82(4), 801-808.
26. DeCastro, M.; Nankova, B.B.; Shah, P.; Patel, P.; Mally, P.V.; Mishra, R.; La Gamma, E.F. Short chain fatty acids regulate tyrosine hydroxylase gene expression through a cAMP-dependent signaling pathway. Brain Res. Mol. Brain Res., 2005, 142(1), 28-38.
27. Guo, Z.; Du, X.; Iacovitti, L. Regulation of tyrosine hydroxylase gene expression during transdifferentiation of striatal neurons: changes in transcription factors binding the AP-1 site. J. Neurosci., 1998, 18(20), 8163-8174.
28. Stork, O.; Hashimoto, T.; Obata, K. Haloperidol activates tyrosine hydroxylase gene-expression in the rat substantia nigra, pars reticulata. Brain Res., 1994, 633(1-2), 213-222.
29. Icard-Liepkalns, C.; Biguet, N.F.; Vyas, S.; Robert, J.J.; Sassone-Corsi, P.; Mallet, J. AP-1 complex and c-fos transcription are involved in TPA provoked and trans-synaptic inductions of the tyrosine hydroxylase gene: insights into long-term regulatory mechanisms. J. Neurosci. Res., 1992, 32(2), 290-298.
30. Jensik, P.J.; Arbogast, L.A. Differential and interactive effects of ligand-bound progesterone receptor a and B isoforms on tyrosine hydroxylase promoter activity. J. Neuroendocrinol., 2011, 23(10), 915-925.
31. Bauer, A.L.; Paulding, W.R.; Striet, J.B.; Schnell, P.O.; Czyzyk-Krzeska, M.F. Endogenous von Hippel-Lindau tumor suppressor protein regulates catecholaminergic phenotype in PC12 cells. Cancer Res., 2002, 62(6), 1682-1687.
32. Paulding, W.R.; Schnell, P.O.; Bauer, A.L.; Striet, J.B.; Nash, J.A.; Kuznetsova, A.V.; Czyzyk-Krzeska, M.F. Regulation of gene expression for neurotransmitters during adaptation to hypoxia in oxygen-sensitive neuroendocrine cells. Microsc. Res. Tech., 2002, 59(3), 178-187.
33. Sun, B.; Sterling, C.R.; Tank, A.W. Chronic nicotine treatment leads to sustained stimulation of tyrosine hydroxylase gene transcription rate in rat adrenal medulla. J. Pharmacol. Exp. Ther., 2003, 304(2), 575-588.
34. Ferrari, M.F.; Coelho, E.F.; Farizatto, K.L.; Chadi, G.; Fior-Chadi, D.R. Modulation of tyrosine hydroxylase, neuropeptide y, glutamate, and substance p in Ganglia and brain areas involved in cardiovascular control after chronic exposure to nicotine. Int. J. Hypertens., 2011, 2011.
35. Sabban, E.L.; Hebert, M.A.; Liu, X.; Nankova, B.; Serova, L. Differential effects of stress on gene transcription factors in catecholaminergic systems. Ann. NY Acad. Sci., 2004, 1032, 130-140.
36. Sabban, E.L.; Nankova, B.B.; Serova, L.I.; Kvetnansky, R.; Liu, X. Molecular regulation of gene expression of catecholamine biosynthetic enzymes by stress: sympathetic ganglia versus adrenal medulla. Ann. NY Acad. Sci., 2004, 1018, 370-377.
37. Hebert, M.A.; Serova, L.I.; Sabban, E.L. Single and repeated immobilization stress differentially trigger induction and phosphorylation of several transcription factors and mitogenactivated protein kinases in the rat locus coeruleus. J. Neurochem., 2005, 95(2), 484-498.
38. Romano, G.; Macaluso, M.; Lucchetti, C.; Iacovitti, L. Transcription and epigenetic profile of the promoter, first exon and first intron of the human tyrosine hydroxylase gene. J. Cell Physiol., 2007, 211(2), 431-438.
39. Kim, H.S.; Park, J.S.; Hong, S.J.; Woo, M.S.; Kim, S.Y.; Kim, K.S. Regulation of the tyrosine hydroxylase gene promoter by histone deacetylase inhibitors. Biochem. Biophys. Res. Commun., 2003, 312(4), 950-957.
40. Yang, J.W.; Choi, E.Y.; Park, M.J.; Lee, M.A. Expression of tyrosine hydroxylase is epigenetically regulated in neural stem cells. Biochem. Biophys. Res. Commun., 2011, 414(4), 712-718.
41. Aranyi, T.; Faucheux, B.A.; Khalfallah, O.; Vodjdani, G.; Biguet, N.F.; Mallet, J.; Meloni, R. The tissue-specific methylation of the human tyrosine hydroxylase gene reveals new regulatory elements in the first exon. J. Neurochem., 2005, 94(1), 129-139.
42. Nagatsu, T. The human tyrosine hydroxylase gene. Cell Mol. Neurobiol., 1989, 9(3), 313-321.
43. Kim, S.J.; Lee, J.W.; Chun, H.S.; Joh, T.H.; Son, J.H. Monitoring catecholamine differentiation in the embryonic brain and peripheral neurons using E. coli lacZ as a reporter gene. Mol. Cells, 1997, 7(3), 394-398.
44. Sawamoto, K.; Nakao, N.; Kobayashi, K.; Matsushita, N.; Takahashi, H.; Kakishita, K.; Yamamoto, A.; Yoshizaki, T.; Terashima, T.; Murakami, F.; Itakura, T.; Okano, H. Visualization, direct isolation, and transplantation of midbrain dopaminergic neurons. Proc. Natl. Acad. Sci. USA, 2001, 98(11), 6423-6428.
45. Zhang, G.R.; Zhao, H.; Li, X.; Awasthi, S.; Geller, A.I. A 16bp upstream sequence from the rat tyrosine hydroxylase promoter supports long-term expression from a neurofilament promoter, in a helper virus-free HSV-1 vector system. Brain Res., 2011, 1415, 109-118.
46. Liu, J.; Merlie, J.P.; Todd, R.D.; O'Malley, K.L. Identification of cell type-specific promoter elements associated with the rat tyrosine hydroxylase gene using transgenic founder analysis. Brain Res. Mol. Brain Res., 1997, 50(1-2), 33-42.
47. Schimmel, J.J.; Crews, L.; Roffler-Tarlov, S.; Chikaraishi, D.M. 4.5 kb of the rat tyrosine hydroxylase 5' flanking sequence directs tissue specific expression during development and contains consensus sites for multiple transcription factors. Brain Res. Mol. Brain Res., 1999, 74(1-2), 1-14.
48. Kim, T.E.; Park, M.J.; Choi, E.J.; Lee, H.S.; Lee, S.H.; Yoon, S.H.; Oh, C.K.; Lee, B.J.; Kim, S.U.; Lee, Y.S.; Lee, M.A. Cloning and cell type-specific regulation of the human tyrosine hydroxylase gene promoter. Biochem. Biophys. Res. Commun., 2003, 312(4), 1123-1131.
49. Cazorla, P.; Smidt, M.P.; O'Malley, K.L.; Burbach, J.P. A response element for the homeodomain transcription factor Ptx3 in the tyrosine hydroxylase gene promoter. J. Neurochem., 2000, 74(5), 1829-1837.
50. Cambi, F.; Fung, B.; Chikaraishi, D. 5' flanking DNA sequences direct cell-specific expression of rat tyrosine hydroxylase. J. Neurochem., 1989, 53(5), 1656-1659.
51. Fung, B.P.; Yoon, S.O.; Chikaraishi, D.M. Sequences that direct rat tyrosine hydroxylase gene expression. J. Neurochem., 1992, 58(6), 2044-2052.
52. Yoon, S.O.; Chikaraishi, D.M. Isolation of two E-box binding factors that interact with the rat tyrosine hydroxylase enhancer. J. Biol. Chem., 1994, 269(28), 18453-18462.
53. 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, 1999, 126(18), 4017-4026.
54. Iwawaki, T.; Kohno, K.; Kobayashi, K. Identification of a potential nurr1 response element that activates the tyrosine hydroxylase gene promoter in cultured cells. Biochem. Biophys. Res. Commun., 2000, 274(3), 590-595.
55. Kim, H.S.; Hong, S.J.; LeDoux, M.S.; Kim, K.S. Regulation of the tyrosine hydroxylase and dopamine beta-hydroxylase genes by the transcription factor AP-2. J. Neurochem., 2001, 76(1), 280-294.
56. Kim, S.M.; Yang, J.W.; Park, M.J.; Lee, J.K.; Kim, S.U.; Lee, Y.S.; Lee, M.A. Regulation of human tyrosine hydroxylase gene by neuron-restrictive silencer factor. Biochem. Biophys. Res. Commun., 2006, 346(2), 426-435.
57. Kelly, B.B.; Hedlund, E.; Kim, C.; Ishiguro, H.; Isacson, O.; Chikaraishi, D.M.; Kim, K.S.; Feng, G. A tyrosine hydroxylaseyellow fluorescent protein knock-in reporter system labeling dopaminergic neurons reveals potential regulatory role for the first intron of the rodent tyrosine hydroxylase gene. Neuroscience, 2006, 142(2), 343-354.
58. Kadkhodaei, B.; Ito, T.; Joodmardi, E.; Mattsson, B.; Rouillard, C.; Carta, M.; Muramatsu, S.; Sumi-Ichinose, C.; Nomura, T.; Metzger, D.; Chambon, P.; Lindqvist, E.; Larsson, N.G.; Olson, L.; Bjorklund, A.; Ichinose, H.; Perlmann, T. Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons. J. Neurosci., 2009, 29(50), 15923-15932.
59. Nunes, M.C.; Roy, N.S.; Keyoung, H.M.; Goodman, R.R.; McKhann, G., 2nd; Jiang, L.; Kang, J.; Nedergaard, M.; Goldman, S.A. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat. Med., 2003, 9(4), 439-447.
60. Sonnier, L.; Le Pen, G.; Hartmann, A.; Bizot, J.C.; Trovero, F.; Krebs, M.O.; Prochiantz, A. Progressive loss of dopaminergic neurons in the ventral midbrain of adult mice heterozygote for Engrailed1. J. Neurosci., 2007, 27(5), 1063-1071.
61. Prakash, N.; Wurst, W. Genetic networks controlling the development of midbrain dopaminergic neurons. J. Physiol., 2006, 575(Pt 2), 403-410.
62. Smidt, M.P.; Smits, S.M.; Burbach, J.P. Molecular mechanisms underlying midbrain dopamine neuron development and function. Eur. J. Pharmacol., 2003, 480(1-3), 75-88.
63. Kim, K.S.; Kim, C.H.; Hwang, D.Y.; Seo, H.; Chung, S.; Hong, S.J.; Lim, J.K.; Anderson, T.; Isacson, O. Orphan nuclear receptor Nurr1 directly transactivates the promoter activity of the tyrosine hydroxylase gene in a cell-specific manner. J. Neurochem., 2003, 85(3), 622-634.
64. Katunar, M.R.; Saez, T.; Brusco, A.; Antonelli, M.C. Ontogenetic expression of dopamine-related transcription factors and tyrosine hydroxylase in prenatally stressed rats. Neurotox Res., 2010, 18(1), 69-81.
65. Lee, H.S.; Bae, E.J.; Yi, S.H.; Shim, J.W.; Jo, A.Y.; Kang, J.S.; Yoon, E.H.; Rhee, Y.H.; Park, C.H.; Koh, H.C.; Kim, H.J.; Choi, H.S.; Han, J.W.; Lee, Y.S.; Kim, J.; Li, J.Y.; Brundin, P.; Lee, S.H. Foxa2 and Nurr1 synergistically yield A9 nigral dopamine neurons exhibiting improved differentiation, function, and cell survival. Stem Cells, 2010, 28(3), 501-512.
66. Maxwell, S.L.; Ho, H.Y.; Kuehner, E.; Zhao, S.; Li, M. Pitx3 regulates tyrosine hydroxylase expression in the substantia nigra and identifies a subgroup of mesencephalic dopaminergic progenitor neurons during mouse development. Dev. Biol., 2005, 282(2), 467-479.
67. Zetterstrom, R.H.; Solomin, L.; Jansson, L.; Hoffer, B.J.; Olson, L.; Perlmann, T. Dopamine neuron agenesis in Nurr1-deficient mice. Science, 1997, 276(5310), 248-250.
68. Messmer, K.; Remington, M.P.; Skidmore, F.; Fishman, P.S. Induction of tyrosine hydroxylase expression by the transcription factor Pitx3. Int. J. Dev. Neurosci., 2007, 25(1), 29-37.
69. Zhong, N.; Kim, C.Y.; Rizzu, P.; Geula, C.; Porter, D.R.; Pothos, E.N.; Squitieri, F.; Heutink, P.; Xu, J. DJ-1 transcriptionally upregulates the human tyrosine hydroxylase by inhibiting the sumoylation of pyrimidine tract-binding protein-associated splicing factor. J. Biol. Chem., 2006, 281(30), 20940-20948.
70. Ishikawa, S.; Taira, T.; Niki, T.; Takahashi-Niki, K.; Maita, C.; Maita, H.; Ariga, H.; Iguchi-Ariga, S.M. Oxidative status of DJ-1-dependent activation of dopamine synthesis through interaction of tyrosine hydroxylase and 4-dihydroxy-L-phenylalanine (L-DOPA) decarboxylase with DJ-1. J. Biol. Chem., 2009, 284(42), 28832-28844.
71. Gandelman, K.Y.; Coker, G.T., 3rd; Moffat, M.; O'Malley, K.L. Species and regional differences in the expression of cell-type specific elements at the human and rat tyrosine hydroxylase gene loci. J. Neurochem., 1990, 55(6), 2149-2152.
72. Jin, H.; Romano, G.; Marshall, C.; Donaldson, A.E.; Suon, S.; Iacovitti, L. Tyrosine hydroxylase gene regulation in human neuronal progenitor cells does not depend on Nurr1 as in the murine and rat systems. J. Cell Physiol., 2006, 207(1), 49-57.
73. Ishikawa, S.; Taira, T.; Takahashi-Niki, K.; Niki, T.; Ariga, H.; Iguchi-Ariga, S.M. Human DJ-1-specific transcriptional activation of tyrosine hydroxylase gene. J. Biol. Chem., 2010, 285(51), 39718-39731.
74. Tondreau, T.; Lagneaux, L.; Dejeneffe, M.; Massy, M.; Mortier, C.; Delforge, A.; Bron, D. Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation. Differentiation, 2004, 72(7), 319-326.
75. Park, C.H.; Minn, Y.K.; Lee, J.Y.; Choi, D.H.; Chang, M.Y.; Shim, J.W.; Ko, J.Y.; Koh, H.C.; Kang, M.J.; Kang, J.S.; Rhie, D.J.; Lee, Y.S.; Son, H.; Moon, S.Y.; Kim, K.S.; Lee, S.H. In vitro and in vivo analyses of human embryonic stem cell-derived dopamine neurons. J. Neurochem., 2005, 92(5), 1265-1276.
76. Hedlund, E.; Pruszak, J.; Ferree, A.; Vinuela, A.; Hong, S.; Isacson, O.; Kim, K.S. Selection of embryonic stem cell-derived enhanced green fluorescent protein-positive dopamine neurons using the tyrosine hydroxylase promoter is confounded by reporter gene expression in immature cell populations. Stem Cells, 2007, 25(5), 1126-1135.