Vesicular monoamine transporter 2 and dopamine transporter are molecular targets of Pitx3 in the ventral midbrain dopamine neurons

Journal of Neurochemistry

Volumn 111, Issue 5, 2009, Pages 1202-1212

  Hwang, Dong Youn ^a,b   Hong, Sunghoi ^a   Jeong, Joo Won ^a   Choi, Sangdun ^c   Kim, Hansoo ^a   Kim, Jangwoo ^a   Kim, Kwang Soo ^a  

^a MCLEAN HOSPITAL   (United States)

^b CHA University   (South Korea)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Aphakia mice; Dopamine neuron; Parkinson's disease; Pitx3; Substantia nigra pars compacta

Indexed keywords

DOPAMINE TRANSPORTER; NUCLEAR RECEPTOR RELATED FACTOR 1; PITX3 PROTEIN; PROTEIN DERIVATIVE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VESICULAR MONOAMINE TRANSPORTER 2;

ANIMAL TISSUE; APHAKIA; ARTICLE; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; DOPAMINERGIC NERVE CELL; EMBRYO; EXPERIMENTAL MOUSE; GENE EXPRESSION; GENE TARGETING; MOLECULAR MECHANICS; MOUSE; NEUROTRANSMISSION; NONHUMAN; PARKINSON DISEASE; PITX3 GENE; PRIORITY JOURNAL; PROTEIN TRANSPORT; SUBSTANTIA NIGRA; VOLUNTARY MOVEMENT; WILD TYPE;

ANIMALS; CELL LINE, TRANSFORMED; CHROMATIN IMMUNOPRECIPITATION; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; EMBRYO, MAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; LEUKEMIA INHIBITORY FACTOR; MESENCEPHALON; MICE; MICE, KNOCKOUT; MICRODISSECTION; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTION FACTORS; VESICULAR MONOAMINE TRANSPORT PROTEINS;

MUS;

EID: 70350782372     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06404.x     Document Type: Article

References (47)

1. Blackwell T. K., Kretzner L., Blackwood E. M., Eisenman R. N. Weintraub H. (1990) Sequence-specific DNA binding by the c-Myc protein. Science 250, 1149 1151.
2. Castillo S. O., Baffi J. S., Palkovits M., Goldstein D. S., Kopin I. J., Witta J., Magnuson M. A. Nikodem V. M. (1998) 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, 36 46.
3. Cazorla P., Smidt M. P., O'Malley K. L. Burbach J. P. (2000) A response element for the homeodomain transcription factor Ptx3 in the tyrosine hydroxylase gene promoter. J. Neurochem. 74, 1829 1837.
4. Chung S., Hedlund E., Hwang M., Kim D. W., Shin B. S., Hwang D. Y., Jung Kang U., Isacson O. Kim K. S. (2005) The homeodomain transcription factor Pitx3 facilitates differentiation of mouse embryonic stem cells into AHD2-expressing dopaminergic neurons. Mol. Cell. Neurosci. 28, 241 252.
5. Fon E. A., Pothos E. N., Sun B. C., Killeen N., Sulzer D. Edwards R. H. (1997) Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action. Neuron 19, 1271 1283.
6. Fuchs J., Mueller J. C., Lichtner P. et al. (2009) The transcription factor PITX3 is associated with sporadic Parkinson's disease. Neurobiol. Aging 30, 731 738.
7. Grimes D. A., Han F., Panisset M., Racacho L., Xiao F., Zou R., Westaff K. Bulman D. E. (2006) Translated mutation in the Nurr1 gene as a cause for Parkinson's disease. Mov. Disord. 21, 906 909.
8. Hanes S. D., Riddihough G., Ish-Horowicz D. Brent R. (1994) Specific DNA recognition and intersite spacing are critical for action of the bicoid morphogen. Mol. Cell. Biol. 14, 3364 3375.
9. Harrington K. A., Augood S. J., Kingsbury A. E., Foster O. J. Emson P. C. (1996) Dopamine transporter (Dat) and synaptic vesicle amine transporter (VMAT2) gene expression in the substantia nigra of control and Parkinson's disease. Brain Res. Mol. Brain Res. 36, 157 162.
10. Hermanson E., Joseph B., Castro D. et al. (2003) Nurr1 regulates dopamine synthesis and storage in MN9D dopamine cells. Exp. Cell Res. 288, 324 334.
11. Hermanson E., Borgius L., Bergsland M., Joodmardi E. Perlmann T. (2006) Neuropilin1 is a direct downstream target of Nurr1 in the developing brain stem. J. Neurochem. 97, 1403 1411.
12. Hwang D. Y., Ardayfio P., Kang U. J., Semina E. V. Kim K. S. (2003) Selective loss of dopaminergic neurons in the substantia nigra of Pitx3-deficient aphakia mice. Brain Res. Mol. Brain Res. 114, 123 131.
13. Hwang D. Y., Fleming S. M., Ardayfio P., Moran-Gates T., Kim H., Tarazi F. I., Chesselet M. F. Kim K. S. (2005) 3,4-dihydroxyphenylalanine reverses the motor deficits in Pitx3-deficient aphakia mice: behavioral characterization of a novel genetic model of Parkinson's disease. J. Neurosci. 25, 2132 2137.
14. Iwawaki T., Kohno K. Kobayashi K. (2000) Identification of a potential nurr1 response element that activates the tyrosine hydroxylase gene promoter in cultured cells. Biochem. Biophys. Res. Commun. 274, 590 595.
15. Jacobs F. M., Smits S. M., Noorlander C. W., von Oerthel L., van der Linden A. J., Burbach J. P. Smidt M. P. (2007) Retinoic acid counteracts developmental defects in the substantia nigra caused by Pitx3 deficiency. Development 134, 2673 2684.
16. Jacobs F. M., van Erp S., van der Linden A. J., von Oerthel L., Burbach J. P. Smidt M. P. (2009) Pitx3 potentiates Nurr1 in dopamine neuron terminal differentiation through release of SMRT-mediated repression. Development 136, 531 540.
17. Jones S. R., Gainetdinov R. R., Hu X. T., Cooper D. C., Wightman R. M., White F. J. Caron M. G. (1999) Loss of autoreceptor functions in mice lacking the dopamine transporter. Nat. Neurosci. 2, 649 655.
18. Joseph B., Wallen-Mackenzie A., Benoit G., Murata T., Joodmardi E., Okret S. Perlmann T. (2003) p57(Kip2) cooperates with Nurr1 in developing dopamine cells. Proc. Natl. Acad. Sci. U.S.A. 100, 15619 15624. (Pubitemid 38021039)
19. Kim K. S., Kim C. H., Hwang D. Y., Seo H., Chung S., Hong S. J., Lim J. K., Anderson T. Isacson O. (2003) Orphan nuclear receptor Nurr1 directly transactivates the promoter activity of the tyrosine hydroxylase gene in a cell-specific manner. J. Neurochem. 85, 622 634.
20. Le W. D., Xu P., Jankovic J., Jiang H., Appel S. H., Smith R. G. Vassilatis D. K. (2003) Mutations in NR4A2 associated with familial Parkinson disease. Nat. Genet. 33, 85 89.
21. Le W., Pan T., Huang M., Xu P., Xie W., Zhu W., Zhang X., Deng H. Jankovic J. (2008) Decreased NURR1 gene expression in patients with Parkinson's disease. J. Neurol. Sci. 273, 29 33.
22. Lee S. H., Lumelsky N., Studer L., Auerbach J. M. McKay R. D. (2000) Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotechnol. 18, 675 679.
23. Luo Y., Henricksen L. A., Giuliano R. E., Prifti L., Callahan L. M. Federoff H. J. (2007) VIP is a transcriptional target of Nurr1 in dopaminergic cells. Exp. Neurol. 203, 221 232.
24. Martinat C., Bacci J. J., Leete T. et al. (2006) Cooperative transcription activation by Nurr1 and Pitx3 induces embryonic stem cell maturation to the midbrain dopamine neuron phenotype. Proc. Natl. Acad. Sci. U.S.A. 103, 2874 2879.
25. Maxwell S. L., Ho H. Y., Kuehner E., Zhao S. Li M. (2005) Pitx3 regulates tyrosine hydroxylase expression in the substantia nigra and identifies a subgroup of mesencephalic dopaminergic progenitor neurons during mouse development. Dev. Biol. 282, 467 479.
26. Messmer K., Remington M. P., Skidmore F. Fishman P. S. (2007) Induction of tyrosine hydroxylase expression by the transcription factor Pitx3. Int. J. Dev. Neurosci. 25, 29 37.
27. Miller G. W., Gainetdinov R. R., Levey A. I. Caron M. G. (1999) Dopamine transporters and neuronal injury. Trends Pharmacol. Sci. 20, 424 429.
28. van den Munckhof P., Luk K. C., Ste-Marie L., Montgomery J., Blanchet P. J., Sadikot A. F. Drouin J. (2003) Pitx3 is required for motor activity and for survival of a subset of midbrain dopaminergic neurons. Development 130 2535 2542.
29. Nunes I., Tovmasian L. T., Silva R. M., Burke R. E. Goff S. P. (2003) Pitx3 is required for development of substantia nigra dopaminergic neurons. Proc. Natl. Acad. Sci. U.S.A. 100, 4245 4250.
30. Peng C., Fan S., Li X., Fan X., Ming M., Sun Z. Le W. (2007) Overexpression of pitx3 upregulates expression of BDNF and GDNF in SH-SY5Y cells and primary ventral mesencephalic cultures. FEBS Lett. 581, 1357 1361.
31. Perrone-Capano C., Tino A. di Porzio U. (1994) Target cells modulate dopamine transporter gene expression during brain development. Neuroreport 5, 1145 1148.
32. Riddle R. Pollock J. D. (2003) Making connections: the development of mesencephalic dopaminergic neurons. Brain Res. Dev. Brain Res. 147, 3 21.
33. Rocha B. A., Fumagalli F., Gainetdinov R. R., Jones S. R., Ator R., Giros B., Miller G. W. Caron M. G. (1998) Cocaine self-administration in dopamine-transporter knockout mice. Nat. Neurosci. 1, 132 137.
34. Roth R. H. Elsworth J. D. (1995) Biochemical pharmacology of midbrain dopamine neurons, in Psychopharmacology: The Fourth Generation of Progress (Bloom F. E. Kupfer D. J., eds pp. 227 243. Raven, New York.
35. Sakurada K., Ohshima-Sakurada M., Palmer T. D. Gage F. H. (1999) Nurr1, an orphan nuclear receptor, is a transcriptional activator of endogenous tyrosine hydroxylase in neural progenitor cells derived from the adult brain. Development 126, 4017 4026.
36. 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. (1998) 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, 4013 4018.
37. Schutz B., Schafer M. K., Eiden L. E. Weihe E. (1998) Vesicular amine transporter expression and isoform selection in developing brain, peripheral nervous system and gut. Brain Res. Dev. Brain Res. 106, 181 204.
38. Semina E. V., Reiter R. S. Murray J. C. (1997) 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, 2109 2116.
39. Shimada S., Kitayama S., Walther D. Uhl G. (1992) Dopamine transporter mRNA: dense expression in ventral midbrain neurons. Brain Res. Mol. Brain Res. 13, 359 362.
40. 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. (1997) A homeodomain gene Ptx3 has highly restricted brain expression in mesencephalic dopaminergic neurons. Proc. Natl. Acad. Sci. U.S.A. 94, 13305 13310.
41. Smidt M. P., Asbreuk C. H., Cox J. J., Chen H., Johnson R. L. Burbach J. P. (2000) A second independent pathway for development of mesencephalic dopaminergic neurons requires Lmx1b. Nat. Neurosci. 3, 337 341.
42. Smidt M. P., Smits S. M., Bouwmeester H., Hamers F. P., van der Linden A. J., Hellemons A. J., Graw J. Burbach J. P. (2004) Early developmental failure of substantia nigra dopamine neurons in mice lacking the homeodomain gene Pitx3. Development 131, 1145 1155.
43. Smits S. M. Smidt M. P. (2006) The role of Pitx3 in survival of midbrain dopaminergic neurons. J. Neural Transm. 70, 57 60.
44. Smits S. M., Ponnio T., Conneely O. M., Burbach J. P. Smidt M. P. (2003) Involvement of Nurr1 in specifying the neurotransmitter identity of ventral midbrain dopaminergic neurons. Eur. J. Neurosci. 18, 1731 1738.
45. Uhl G. R., Walther D., Mash D., Faucheux B. Javoy-Agid F. (1994) Dopamine transporter messenger RNA in Parkinson's disease and control substantia nigra neurons. Ann. Neurol. 35, 494 498.
46. Volpicelli F., Caiazzo M., Greco D., Consales C., Leone L., Perrone-Capano C., D'Amato L. C. Porzio U. (2007) Bdnf gene is a downstream target of Nurr1 transcription factor in rat midbrain neurons in vitro. J. Neurochem. 102, 441 453.
47. Wallen A. A., Castro D. S., Zetterstrom R. H., Karlen M., Olson L., Ericson J. Perlmann T. (2001) Orphan nuclear receptor Nurr1 is essential for Ret expression in midbrain dopamine neurons and in the brain stem. Mol. Cell. Neurosci. 18, 649 663.