Transcription factors Foxa1 and Foxa2 are required for adult dopamine neurons maintenance

Frontiers in Cellular Neuroscience

Volumn 8, Issue SEP, 2014, Pages

  Domanskyi, Andrii ^a,c   Alter, Heike ^a   Vogt, Miriam A ^b   Gass, Peter ^b   Vinnikov, Ilya A ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Dopamine; Dopaminergic neurons; Foxa1; Foxa2; Neurodegeneration; Parkinson s disease; Substantia nigra; Transgenic mice

Indexed keywords

AROMATIC LEVO AMINO ACID DECARBOXYLASE; DOPAMINE TRANSPORTER; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; HEPATOCYTE NUCLEAR FACTOR 3BETA; REACTIVE OXYGEN METABOLITE; TAMOXIFEN; UNCOUPLING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOWN REGULATION; EMBRYO DEVELOPMENT; GENE CONTROL; GENE DELETION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE DEGENERATION; NONHUMAN; OPEN FIELD TEST; PARKINSON DISEASE; PHENOTYPE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAROD TEST; UPREGULATION;

EID: 84908217465     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00275     Document Type: Article

References (57)

1. Abou-Sleiman, P. M., Muqit, M. M., and Wood, N. W. (2006). Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat. Rev. Neurosci. 7, 207-219. doi: 10.1038/nrn1868
2. Allain, H., Bentue-Ferrer, D., and Akwa, Y. (2008). Disease-modifying drugs and Parkinson's disease. Prog. Neurobiol. 84, 25-39. doi: 10.1016/j.pneurobio.2007.10.003
3. Anderson, D. W., Schray, R. C., Duester, G., and Schneider, J. S. (2011). Functional significance of aldehyde dehydrogenase ALDH1A1 to the nigrostriatal dopamine system. Brain Res. 1408, 81-87. doi: 10.1016/j.brainres.2011.06.051
4. Andrews, Z. B., Horvath, B., Barnstable, C. J., Elsworth, J., Yang, L., Beal, M. F., et al. (2005). Uncoupling protein-2 is critical for nigral dopamine cell survival in a mouse model of Parkinson's disease. J. Neurosci. 25, 184-191. doi: 10.1523/JNEUROSCI.4269-04.2005
5. Braak, H., Del Tredici, K., Rub, U., De Vos, R. A., Jansen Steur, E. N., and Braak, E. (2003). Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 24, 197-211. doi: 10.1016/S0197-4580(02)00065-9
6. Brooks, S. P., and Dunnett, S. B. (2009). Tests to assess motor phenotype in mice: a user's guide. Nat. Rev. Neurosci. 10, 519-529. doi: 10.1038/nrn2652
7. Chourbaji, S., Brandwein, C., Vogt, M. A., Dormann, C., Hellweg, R., and Gass, P. (2008). Nature vs. nurture: can enrichment rescue the behavioural phenotype of BDNF heterozygous mice? Behav. Brain Res. 192, 254-258. doi: 10.1016/j.bbr.2008.04.015
8. Conti, B., Sugama, S., Lucero, J., Winsky-Sommerer, R., Wirz, S. A., Maher, P., et al. (2005). Uncoupling protein 2 protects dopaminergic neurons from acute 1,2,3,6-methyl-phenyl-tetrahydropyridine toxicity. J. Neurochem. 93, 493-501. doi: 10.1111/j.1471-4159.2005.03052.x
9. Di Giovannantonio, L. G., Di Salvio, M., Acampora, D., Prakash, N., Wurst, W., and Simeone, A. (2013). Otx2 selectively controls the neurogenesis of specific neuronal subtypes of the ventral tegmental area and compensates En1-dependent neuronal loss and MPTP vulnerability. Dev. Biol. 373, 176-183. doi: 10.1016/j.ydbio.2012.10.022
10. Di Salvio, M., Di Giovannantonio, L. G., Acampora, D., Prosperi, R., Omodei, D., Prakash, N., et al. (2010). Otx2 controls neuron subtype identity in ventral tegmental area and antagonizes vulnerability to MPTP. Nat. Neurosci. 13, 1481-1488. doi: 10.1038/nn.2661
11. Domanskyi, A., Geissler, C., Vinnikov, I. A., Alter, H., Schober, A., Vogt, M. A., et al. (2011). Pten ablation in adult dopaminergic neurons is neuroprotective in Parkinson's disease models. FASEB J. 25, 2898-2910. doi: 10.1096/fj.11-181958
12. Engblom, D., Bilbao, A., Sanchis-Segura, C., Dahan, L., Perreau-Lenz, S., Balland, B., et al. (2008). Glutamate receptors on dopamine neurons control the persistence of cocaine seeking. Neuron 59, 497-508. doi: 10.1016/j.neuron.2008.07.010
13. Enkel, T., Berger, S. M., Schonig, K., Tews, B., and Bartsch, D. (2014). Reduced expression of nogo-a leads to motivational deficits in rats. Front. Behav. Neurosci. 8:10. doi: 10.3389/fnbeh.2014.00010
14. Ferri, A. L., Lin, W., Mavromatakis, Y. E., Wang, J. C., Sasaki, H., Whitsett, J. A., et al. (2007). Foxa1 and Foxa2 regulate multiple phases of midbrain dopaminergic neuron development in a dosage-dependent manner.Development 134, 2761-2769. doi: 10.1242/dev.000141
15. Friedman, J. R., and Kaestner, K. H. (2006). The Foxa family of transcription factors in development and metabolism. Cell. Mol. Life Sci. 63, 2317-2328. doi: 10.1007/s00018-006-6095-6
16. Gao, N., Lelay, J., Vatamaniuk, M. Z., Rieck, S., Friedman, J. R., and Kaestner, K. H. (2008). Dynamic regulation of Pdx1 enhancers by Foxa1 and Foxa2 is essential for pancreas development. Genes Dev. 22, 3435-3448. doi: 10.1101/gad.1752608
17. Hauser, M. A., Li, Y. J., Xu, H., Noureddine, M. A., Shao, Y. S., Gullans, S. R., et al. (2005). Expression profiling of substantia nigra in Parkinson disease, progressive supranuclear palsy, and frontotemporal dementia with parkinsonism. Arch. Neurol. 62, 917-921. doi: 10.1001/archneur.62.6.917
18. Heuer, A., Smith, G. A., Lelos, M. J., Lane, E. L., and Dunnett, S. B. (2012). Unilateral nigrostriatal 6-hydroxydopamine lesions in mice I: motor impairments identify extent of dopamine depletion at three different lesion sites. Behav. Brain Res. 228, 30-43. doi: 10.1016/j.bbr.2011.11.027
19. Isermann, B., Vinnikov, I. A., Madhusudhan, T., Herzog, S., Kashif, M., Blautzik, J., et al. (2007). Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis. Nat. Med. 13, 1349-1358. doi: 10.1038/nm1667
20. Jacobs, F. M., Van Erp, S., Van Der Linden, A. J., Von Oerthel, L., Burbach, J. P., and Smidt, M. P. (2009). Pitx3 potentiates Nurr1 in dopamine neuron terminal differentiation through release of SMRT-mediated repression.Development 136, 531-540. doi: 10.1242/dev.029769
21. Joksimovic, M., Anderegg, A., Roy, A., Campochiaro, L., Yun, B., Kittappa, R., et al. (2009). Spatiotemporally separable Shh domains in the midbrain define distinct dopaminergic progenitor pools. Proc. Natl. Acad. Sci. U.S.A. 106, 19185-19190. doi: 10.1073/pnas.0904285106
22. Kadkhodaei, B., Alvarsson, A., Schintu, N., Ramskold, D., Volakakis, N., Joodmardi, E., et al. (2013). Transcription factor Nurr1 maintains fiber integrity and nuclear-encoded mitochondrial gene expression in dopamine neurons.Proc. Natl. Acad. Sci. U.S.A. 110, 2360-2365. doi: 10.1073/pnas.1221077110
23. Kadkhodaei, B., Ito, T., Joodmardi, E., Mattsson, B., Rouillard, C., Carta, M., et al. (2009). Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons. J. Neurosci. 29, 15923-15932. doi: 10.1523/JNEUROSCI.3910-09.2009
24. Kaestner, K. H. (2010). The FoxA factors in organogenesis and differentiation. Curr. Opin. Genet. Dev. 20, 527-532. doi: 10.1016/j.gde.2010.06.005
25. Kittappa, R., Chang, W. W., Awatramani, R. B., and McKay, R. D. (2007). The foxa2 gene controls the birth and spontaneous degeneration of dopamine neurons in old age. PLoS Biol. 5:e325. doi: 10.1371/journal.pbio.0050325
26. Klucken, J., Shin, Y., Masliah, E., Hyman, B. T., and McLean, P. J. (2004). Hsp70 Reduces alpha-Synuclein aggregation and toxicity. J. Biol. Chem. 279, 25497-25502. doi: 10.1074/jbc.M400255200
27. Lai, E., Prezioso, V. R., Tao, W. F., Chen, W. S., and Darnell, J. E. Jr. (1991). Hepatocyte nuclear factor 3 alpha belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Dev. 5, 416-427. doi: 10.1101/gad.5.3.416
28. Lee, H. S., Bae, E. J., Yi, S. H., Shim, J. W., Jo, A. Y., Kang, J. S., et al. (2010). Foxa2 and Nurr1 synergistically yield A9 nigral dopamine neurons exhibiting improved differentiation, function, and cell survival. Stem Cells 28, 501-512. doi: 10.1002/stem.29
29. Lesnick, T. G., Papapetropoulos, S., Mash, D. C., Ffrench-Mullen, J., Shehadeh, L., De Andrade, M., et al. (2007). A genomic pathway approach to a complex disease: axon guidance and Parkinson disease. PLoS Genet. 3:e98. doi: 10.1371/journal.pgen.0030098
30. Lin, W., Metzakopian, E., Mavromatakis, Y. E., Gao, N., Balaskas, N., Sasaki, H., et al. (2009). Foxa1 and Foxa2 function both upstream of and cooperatively with Lmx1a and Lmx1b in a feedforward loop promoting mesodiencephalic dopaminergic neuron development. Dev. Biol. 333, 386-396. doi: 10.1016/j.ydbio.2009.07.006
31. Liu, G., Yu, J., Ding, J., Xie, C., Sun, L., Rudenko, I., et al. (2014). Aldehyde dehydrogenase 1 defines and protects a nigrostriatal dopaminergic neuron subpopulation. J. Clin. Invest. 124, 3032-3046. doi: 10.1172/JCI72176
32. Marchitti, S. A., Deitrich, R. A., and Vasiliou, V. (2007). Neurotoxicity and metabolism of the catecholamine-derived 3,4-dihydroxyphenylacetaldehyde and 3,4-dihydroxyphenylglycolaldehyde: the role of aldehyde dehydrogenase. Pharmacol. Rev. 59, 125-150. doi: 10.1124/pr.59.2.1
33. Meissner, W. G., Frasier, M., Gasser, T., Goetz, C. G., Lozano, A., Piccini, P., et al. (2011). Priorities in Parkinson's disease research. Nat. Rev. Drug Discov. 10, 377-393. doi: 10.1038/nrd3430
34. Mesman, S., Von Oerthel, L., and Smidt, M. P. (2014). Mesodiencephalic dopaminergic neuronal differentiation does not involve gli2a-mediated shh-signaling and is under the direct influence of canonical wnt signaling. PLoS ONE 9:e97926. doi: 10.1371/journal.pone.0097926
35. Monville, C., Torres, E. M., and Dunnett, S. B. (2006). Comparison of incremental and accelerating protocols of the rotarod test for the assessment of motor deficits in the 6-OHDA model. J. Neurosci. Methods 158, 219-223. doi: 10.1016/j.jneumeth.2006.06.001
36. Moore, D. J., West, A. B., Dawson, V. L., and Dawson, T. M. (2005). Molecular pathophysiology of Parkinson's disease. Annu. Rev. Neurosci. 28, 57-87. doi: 10.1146/annurev.neuro.28.061604.135718
37. Moran, L. B., Duke, D. C., Deprez, M., Dexter, D. T., Pearce, R. K., and Graeber, M. B. (2006). Whole genome expression profiling of the medial and lateral substantia nigra in Parkinson's disease. Neurogenetics 7, 1-11. doi: 10.1007/s10048-005-0020-2
38. Omodei, D., Acampora, D., Mancuso, P., Prakash, N., Di Giovannantonio, L. G., Wurst, W., et al. (2008). Anterior-posterior graded response to Otx2 controls proliferation and differentiation of dopaminergic progenitors in the ventral mesencephalon. Development 135, 3459-3470. doi: 10.1242/dev.027003
39. Otto, D., and Unsicker, K. (1990). Basic FGF reverses chemical and morphological deficits in the nigrostriatal system of MPTP-treated mice. J. Neurosci. 10, 1912-1921.
40. Pahwa, R., and Lyons, K. E. (2014). Treatment of early Parkinson's disease. Curr. Opin. Neurol. 27, 442-449. doi: 10.1097/WCO.0000000000000113
41. Perlmann, T., and Wallen-Mackenzie, A. (2004). Nurr1, an orphan nuclear receptor with essential functions in developing dopamine cells. Cell Tissue Res. 318, 45-52. doi: 10.1007/s00441-004-0974-7
42. Rieker, C., Engblom, D., Kreiner, G., Domanskyi, A., Schober, A., Stotz, S., et al. (2011). Nucleolar disruption in dopaminergic neurons leads to oxidative damage and parkinsonism through repression of mammalian target of rapamycin signaling. J. Neurosci. 31, 453-460. doi: 10.1523/JNEUROSCI.0590-10.2011
43. Scherzer, C. R., Eklund, A. C., Morse, L. J., Liao, Z., Locascio, J. J., Fefer, D., et al. (2007). Molecular markers of early Parkinson's disease based on gene expression in blood. Proc. Natl. Acad. Sci. U.S.A. 104, 955-960. doi: 10.1073/pnas.0610204104
44. Smidt, M. P., and Burbach, J. P. H. (2007). How to make a mesodiencephalic dopaminergic neuron. Nat. Rev. Neurosci. 8, 21-32. doi: 10.1038/nrn2039
45. Soccio, R. E., Tuteja, G., Everett, L. J., Li, Z., Lazar, M. A., and Kaestner, K. H. (2011). Species-specific strategies underlying conserved functions of metabolic transcription factors. Mol. Endocrinol. 25, 694-706. doi: 10.1210/me.2010-0454
46. Stott, S. R., Metzakopian, E., Lin, W., Kaestner, K. H., Hen, R., and Ang, S. L. (2013). Foxa1 and foxa2 are required for the maintenance of dopaminergic properties in ventral midbrain neurons at late embryonic stages. J. Neurosci. 33, 8022-8034. doi: 10.1523/JNEUROSCI.4774-12.2013
47. Sund, N. J., Ang, S. L., Sackett, S. D., Shen, W., Daigle, N., Magnuson, M. A., et al. (2000). Hepatocyte nuclear factor 3beta (Foxa2) is dispensable for maintaining the differentiated state of the adult hepatocyte. Mol. Cell. Biol. 20, 5175-5183. doi: 10.1128/MCB.20.14.5175-5183.2000
48. Sutherland, G. T., Matigian, N. A., Chalk, A. M., Anderson, M. J., Silburn, P. A., Mackay-Sim, A., et al. (2009). A cross-study transcriptional analysis of Parkinson's disease. PLoS ONE 4:e4955. doi: 10.1371/journal.pone.0004955
49. Taccioli, C., Tegner, J., Maselli, V., Gomez-Cabrero, D., Altobelli, G., Emmett, W., et al. (2011). ParkDB: a Parkinson's disease gene expression database. Database (Oxford) 2011:bar007. doi: 10.1093/database/bar007
50. Taylor, T. N., Greene, J. G., and Miller, G. W. (2010). Behavioral phenotyping of mouse models of Parkinson's disease. Behav. Brain Res. 211, 1-10. doi: 10.1016/j.bbr.2010.03.004
51. Vinnikov, I. A., Hajdukiewicz, K., Reymann, J., Beneke, J., Czajkowski, R., Roth, L. C., et al. (2014). Hypothalamic miR-103 protects from hyperphagic obesity in mice. J. Neurosci. 34, 10659-10674. doi: 10.1523/JNEUROSCI.4251-13.2014
52. Vogt, I. R., Lees, A. J., Evert, B. O., Klockgether, T., Bonin, M., and Wullner, U. (2006). Transcriptional changes in multiple system atrophy and Parkinson's disease putamen. Exp. Neurol. 199, 465-478. doi: 10.1016/j.expneurol.2006.01.008
53. Wey, M. C., Fernandez, E., Martinez, P. A., Sullivan, P., Goldstein, D. S., and Strong, R. (2012). Neurodegeneration and motor dysfunction in mice lacking cytosolic and mitochondrial aldehyde dehydrogenases: implications for Parkinson's disease. PLoS ONE 7:e31522. doi: 10.1371/journal.pone.0031522
54. Yang, J. H., Li, J. H., Jiang, S., Zhou, H., and Qu, L. H. (2013). ChIPBase: a database for decoding the transcriptional regulation of long non-coding RNA and microRNA genes from ChIP-Seq data. Nucleic Acids Res. 41, D177-D187. doi: 10.1093/nar/gks1060
55. Youdim, M. B. (2010). Why do we need multifunctional neuroprotective and neurorestorative drugs for Parkinson's and Alzheimer's diseases as disease modifying agents. Exp. Neurobiol. 19, 1-14. doi: 10.5607/en.2010.19.1.1
56. Zaborszky, L., and Vadasz, C. (2001). The midbrain dopaminergic system: anatomy and genetic variation in dopamine neuron number of inbred mouse strains. Behav. Genet. 31, 47-59. doi: 10.1023/A:1010257808945
57. Zhang, Y., James, M., Middleton, F. A., and Davis, R. L. (2005). Transcriptional analysis of multiple brain regions in Parkinson's disease supports the involvement of specific protein processing, energy metabolism, and signaling pathways, and suggests novel disease mechanisms. Am. J. Med. Genet. B Neuropsychiatr. Genet. 137B, 5-16. doi: 10.1002/ajmg.b.30195