Vitamin D: A potent regulator of dopaminergic neuron differentiation and function.
differentiation
dopamine
fluorescent false neurotransmitter
vitamin D
Journal
Journal of neurochemistry
ISSN: 1471-4159
Titre abrégé: J Neurochem
Pays: England
ID NLM: 2985190R
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
revised:
23
03
2023
received:
08
12
2022
accepted:
03
04
2023
medline:
24
8
2023
pubmed:
21
4
2023
entrez:
21
04
2023
Statut:
ppublish
Résumé
Vitamin D has been identified as a key factor in dopaminergic neurogenesis and differentiation. Consequently, developmental vitamin D (DVD) deficiency has been linked to disorders of abnormal dopamine signalling with a neurodevelopmental basis such as schizophrenia. Here we provide further evidence of vitamin D's role as a mediator of dopaminergic development by showing that it increases neurite outgrowth, neurite branching, presynaptic protein re-distribution, dopamine production and functional release in various in vitro models of developing dopaminergic cells including SH-SY5Y cells, primary mesencephalic cultures and mesencephalic/striatal explant co-cultures. This study continues to establish vitamin D as an important differentiation agent for developing dopamine neurons, and now for the first time shows chronic exposure to the active vitamin D hormone increases the capacity of developing neurons to release dopamine. This study also has implications for understanding mechanisms behind the link between DVD deficiency and schizophrenia.
Substances chimiques
Vitamin D
1406-16-2
Dopamine
VTD58H1Z2X
Vitamins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
779-789Informations de copyright
© 2023 The Authors. Journal of Neurochemistry published by John Wiley & Sons Ltd on behalf of International Society for Neurochemistry.
Références
Aparecida Nedel Pertile, R., Kiltschewskij, D., Geaghan, M., Barnett, M., Cui, X., Cairns, M. J., & Eyles, D. (2022). Developmental vitamin D-deficiency increases the expression of microRNAs involved in dopamine neuron development. Brain Research, 1789, 147953. https://doi.org/10.1016/j.brainres.2022.147953
Banerjee, A., Imig, C., Balakrishnan, K., Kershberg, L., Lipstein, N., Uronen, R. L., Wang, J., Cai, X., Benseler, F., Rhee, J. S., Cooper, B. H., Liu, C., Wojcik, S. M., Brose, N., & Kaeser, P. S. (2022). Molecular and functional architecture of striatal dopamine release sites. Neuron, 110(2), 248-265.e9. https://doi.org/10.1016/j.neuron.2021.10.028
Black, C. A., Bucher, M. L., Bradner, J. M., Jonas, L., Igarza, K., & Miller, G. W. (2021). Assessing vesicular monoamine transport and toxicity using fluorescent false neurotransmitters. Chemical Research in Toxicology, 34(5), 1256-1264. https://doi.org/10.1021/acs.chemrestox.0c00380
Brown, J., Bianco, J. I., McGrath, J. J., & Eyles, D. W. (2003). 1,25-dihydroxyvitamin D3 induces nerve growth factor, promotes neurite outgrowth and inhibits mitosis in embryonic rat hippocampal neurons. Neuroscience Letters, 343(2), 139-143.
Buckley, K., & Kelly, R. B. (1985). Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. The Journal of Cell Biology, 100(4), 1284-1294. https://doi.org/10.1083/jcb.100.4.1284
Cass, W. A., Peters, L. E., Fletcher, A. M., & Yurek, D. M. (2014). Calcitriol promotes augmented dopamine release in the lesioned striatum of 6-hydroxydopamine treated rats. Neurochemical Research, 39(8), 1467-1476. https://doi.org/10.1007/s11064-014-1331-1
Cui, X., Lefevre, E., Turner, K. M., Coelho, C. M., Alexander, S., Burne, T. H., & Eyles, D. W. (2015). MK-801-induced behavioural sensitisation alters dopamine release and turnover in rat prefrontal cortex. Psychopharmacology, 232(3), 509-517. https://doi.org/10.1007/s00213-014-3689-9
Cui, X., McGrath, J. J., Burne, T. H. J., & Eyles, D. W. (2021). Vitamin D and schizophrenia: 20 years on. Molecular Psychiatry, 26, 2708-2720. https://doi.org/10.1038/s41380-021-01025-0
Cui, X., Pelekanos, M., Burne, T. H., McGrath, J. J., & Eyles, D. W. (2010). Maternal vitamin D deficiency alters the expression of genes involved in dopamine specification in the developing rat mesencephalon. Neuroscience Letters, 486(3), 220-223. S0304-3940(10)01274-7[pii]10.1016/j.neulet.2010.09.057
Cui, X., Pertile, R., Liu, P., & Eyles, D. W. (2015). Vitamin D regulates tyrosine hydroxylase expression: N-cadherin a possible mediator. Neuroscience, 304, 90-100. https://doi.org/10.1016/j.neuroscience.2015.07.048
Dardou, D., Dassesse, D., Cuvelier, L., Deprez, T., De Ryck, M., & Schiffmann, S. N. (2011). Distribution of SV2C mRNA and protein expression in the mouse brain with a particular emphasis on the basal ganglia system. Brain Research, 1367, 130-145. https://doi.org/10.1016/j.brainres.2010.09.063
Dunn, A. R., Stout, K. A., Ozawa, M., Lohr, K. M., Hoffman, C. A., Bernstein, A. I., Li, Y., Wang, M., Sgobio, C., Sastry, N., Cai, H., Caudle, W. M., & Miller, G. W. (2017). Synaptic vesicle glycoprotein 2C (SV2C) modulates dopamine release and is disrupted in Parkinson disease. Proceedings of the National Academy of Sciences of the United States of America, 114(11), E2253-E2262. https://doi.org/10.1073/pnas.1616892114
Eyles, D., Brown, J., Mackay-Sim, A., McGrath, J., & Feron, F. (2003). Vitamin D3 and brain development. Neuroscience, 118(3), 641-653.
Eyles, D., Feldon, J., & Meyer, U. (2012). Schizophrenia: Do all roads lead to dopamine or is this where they start? Evidence from two epidemiologically informed developmental rodent models. Translational Psychiatry, 2, e81. https://doi.org/10.1038/tp.2012.6
Eyles, D. W. (2021a). How do established developmental risk-factors for schizophrenia change the way the brain develops? Translational Psychiatry, 11(1), 158. https://doi.org/10.1038/s41398-021-01273-2
Eyles, D. W. (2021b). Vitamin D: Brain and behavior. JBMR Plus, 5(1), e10419. https://doi.org/10.1002/jbm4.10419
Eyles, D. W., Trzaskowski, M., Vinkhuyzen, A. A. E., Mattheisen, M., Meier, S., Gooch, H., Anggono, V., Cui, X., Tan, M. C., Burne, T. H. J., Jang, S. E., Kvaskoff, D., Hougaard, D. M., Nørgaard-Pedersen, B., Cohen, A., Agerbo, E., Pedersen, C. B., Børglum, A. D., Mors, O., … McGrath, J. J. (2018). The association between neonatal vitamin D status and risk of schizophrenia. Scientific Reports, 8(1), 17692. https://doi.org/10.1038/s41598-018-35418-z
Gooch, H., Cui, X., Anggono, V., Trzaskowski, M., Tan, M. C., Eyles, D. W., Burne, T. H. J., Jang, S. E., Mattheisen, M., Hougaard, D. M., Pedersen, B. N., Cohen, A., Mortensen, P. B., Sah, P., & McGrath, J. J. (2019). 1,25-Dihydroxyvitamin D modulates L-type voltage-gated calcium channels in a subset of neurons in the developing mouse prefrontal cortex. Transl Psychiatry, 9(1), 281. https://doi.org/10.1038/s41398-019-0626-z
Granholm, A. C., Reyland, M., Albeck, D., Sanders, L., Gerhardt, G., Hoernig, G., Shen, L., Westphal, H., & Hoffer, B. (2000). Glial cell line-derived neurotrophic factor is essential for postnatal survival of midbrain dopamine neurons. The Journal of Neuroscience, 20(9), 3182-3190. https://doi.org/10.1523/JNEUROSCI.20-09-03182.2000
Hu, L., Savy, A., Grimaud, L., Guille-Collignon, M., Lemaitre, F., Amatore, C., & Delacotte, J. (2019). Electroactive fluorescent false neurotransmitter FFN102 partially replaces dopamine in PC12 cell vesicles. Biophysical Chemistry, 245, 1-5. https://doi.org/10.1016/j.bpc.2018.11.001
Jeong, H., Kim, M. S., Kim, S. W., Kim, K. S., & Seol, W. (2006). Regulation of tyrosine hydroxylase gene expression by retinoic acid receptor. Journal of Neurochemistry, 98(2), 386-394. https://doi.org/10.1111/j.1471-4159.2006.03866.x
Lezzi, M., Theander, S., Janz, R., Loze, C., & Wollheim, C. B. (2005). SV2A and SV2C are not vesicular Ca2+ transporters but control glucose-evoked granule recruitment. Journal of Cell Science, 118(23), 5647-5660. https://doi.org/10.1242/jcs.02658
Liu, C., Kershberg, L., Wang, J., Schneeberger, S., & Kaeser, P. S. (2018). Dopamine secretion is mediated by sparse active zone-like release sites. Cell, 172(4), 706-718 e715. https://doi.org/10.1016/j.cell.2018.01.008
Luan, W., Hammond, L. A., Cotter, E., Osborne, G. W., Alexander, S. A., Nink, V., Cui, X., & Eyles, D. W. (2018). Developmental vitamin D (DVD) deficiency reduces Nurr1 and TH expression in post-mitotic dopamine neurons in rat mesencephalon. Molecular Neurobiology, 55(3), 2443-2453. https://doi.org/10.1007/s12035-017-0497-3
McCutcheon, R., Beck, K., Jauhar, S., & Howes, O. D. (2018). Defining the locus of dopaminergic dysfunction in schizophrenia: A Meta-analysis and test of the mesolimbic hypothesis. Schizophrenia Bulletin, 44(6), 1301-1311. https://doi.org/10.1093/schbul/sbx180
McGrath, J. J., Eyles, D. W., Pedersen, C. B., Anderson, C., Ko, P., Burne, T. H., Norgaard-Pedersen, B., Hougaard D.M., & Mortensen, P. B. (2010). Neonatal vitamin D status and risk of schizophrenia: A population-based case-control study. Archives of General Psychiatry, 67(9), 889-894. 67/9/889[pii]10.1001/archgenpsychiatry.2010.110
Orme, R. P., Bhangal, M. S., & Fricker, R. A. (2013). Calcitriol imparts neuroprotection in vitro to midbrain dopaminergic neurons by upregulating GDNF expression. PLoS One, 23(8), e62040. https://doi.org/10.1371/journal.pone.0062040
Pereira, D. B., Schmitz, Y., Mészáros, J., Merchant, P., Hu, G., Li, S., Henke, A., Lizardi-Ortiz, J. E., Karpowicz, R. J., Jr., Morgenstern, T. J., Sonders, M. S., Kanter, E., Rodriguez, P. C., Mosharov, E. V., Sames, D., & Sulzer, D. (2016). Fluorescent false neurotransmitter reveals functionally silent dopamine vesicle clusters in the striatum. Nature Neuroscience, 19(4), 578-586. https://doi.org/10.1038/nn.4252
Pertile, R., Cui, X., Hammond, L. A., & Eyles, D. W. (2018). Vitamin D regulation of GDNF/ret signaling in dopaminergic neurons. The FASEB Journal, 32(2), 819-828.
Pertile, R. A. N., Cui, X., & Eyles, D. W. (2016). Vtiamin D signalling and the differentiation of developing dopamine systems. Neuroscience, 333, 193-203. https://doi.org/10.1016/j.neuroscience.2016.07.020
Petty, A., Cui, X., Tesiram, Y., Kirik, D., Howes, O., & Eyles, D. (2019). Enhanced dopamine in prodromal schizophrenia (EDiPS): A new animal model of relevance to schizophrenia. NPJ Schizophrenia, 5(1), 6. https://doi.org/10.1038/s41537-019-0074-z
Schivell, A. E., Mochida, S., Kensel-Hammes, P., Custer, K. L., & Bajjalieh, S. M. (2005). SV2A and SV2C contain a unique synaptotagmin-binding site. Molecular and Cellular Neurosciences, 29(1), 56-64. https://doi.org/10.1016/j.mcn.2004.12.011
Schmidt, E. R., Morello, F., & Pasterkamp, R. J. (2012). Dissection and culture of mouse dopaminergic and striatal explants in three-dimensional collagen matrix assays. Journal of Visualized Experiments, 61. https://doi.org/10.3791/3691
Schmitz, S. K., Hjorth, J. J., Joemai, R. M., Wijntjes, R., Eijgenraam, S., de Bruijn, P., Georgiou, C., de Jong, A. P., van Ooyen, A., Verhage, M., Cornelisse, L. N., Toonen, R. F., & Veldkamp, W. J. (2011). Automated analysis of neuronal morphology, synapse number and synaptic recruitment. Journal of Neuroscience Methods, 195(2), 185-193. https://doi.org/10.1016/j.jneumeth.2010.12.011
Shirazi, H. A., Rasouli, J., Ciric, B., Rostami, A., & Zhang, G. X. (2015). 1,25-Dihydroxyvitamin D3 enhances neural stem cell proliferation and oligodendrocyte differentiation. Experimental and Molecular Pathology, 98(2), 240-245. https://doi.org/10.1016/j.yexmp.2015.02.004
Timms, P. M., Mannan, N., Hitman, G. A., Noonan, K., Mills, P. G., Syndercombe-Court, D., Aganna, E., Price, C. P., & Boucher, B. J. (2002). Circulating MMP9, vitamin D and variation in the TIMP-1 response with VDR genotype: mechanisms for inflammatory damage in chronic disorders? QJM: An International Journal of Medicine, 95(12), 787-796. https://doi.org/10.1093/qjmed/95.12.787
Trinko, J. R., Land, B. B., Solecki, W. B., Wickham, R. J., Tellez, L. A., Maldonado-Aviles, J., de Araujo, I. E., Addy, N. A., & DiLeone, R. J. (2016). Vitamin D3: A role in dopamine circuit regulation, diet-induced obesity, and drug consumption. eNeuro, 3(3), ENEURO.0122-15.2016. https://doi.org/10.1523/ENEURO.0122-15.2016
Weinberger, D. R. (2017). Future of days past: Neurodevelopment and schizophrenia. Schizophrenia Bulletin, 43(6), 1164-1168. https://doi.org/10.1093/schbul/sbx118