{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T15:56:08Z","timestamp":1790697368165,"version":"4.1.0"},"reference-count":63,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,2,5]],"date-time":"2019-02-05T00:00:00Z","timestamp":1549324800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2019,2,5]],"date-time":"2019-02-05T00:00:00Z","timestamp":1549324800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Midbrain dopaminergic (DA) neurons are involved in diverse neurological functions, including control of movements, emotions or reward. In turn, their dysfunctions cause severe clinical manifestations in humans, such as the appearance of motor and cognitive symptoms in Parkinson\u2019s Disease. The physiology and pathophysiology of these neurons are widely studied, mostly with respect to molecular mechanisms implicating protein-coding genes. In contrast, the contribution of non-coding elements of the genome to DA neuron function is poorly investigated. In this study, we isolated DA neurons from E14.5 ventral mesencephalons in mice, and used RNA-seq and ATAC-seq to establish and describe repertoires of long non-coding RNAs (lncRNAs) and putative DNA regulatory regions specific to this neuronal population. We identified 1,294 lncRNAs constituting the repertoire of DA neurons, among which 939 were novel. Most of them were not found in hindbrain serotonergic (5-HT) neurons, indicating a high degree of cell-specificity. This feature was also observed regarding open chromatin regions, as 39% of the ATAC-seq peaks from the DA repertoire were not detected in the 5-HT neurons. Our work provides for the first time DA-specific catalogues of non-coding elements of the genome that will undoubtedly participate in deepening our knowledge regarding DA neuronal development and dysfunctions.<\/jats:p>","DOI":"10.1038\/s41598-018-37872-1","type":"journal-article","created":{"date-parts":[[2019,2,5]],"date-time":"2019-02-05T11:04:11Z","timestamp":1549364651000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Long non-coding RNA repertoire and open chromatin regions constitute midbrain dopaminergic neuron - specific molecular signatures"],"prefix":"10.1038","volume":"9","author":[{"given":"J.","family":"Gendron","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C.","family":"Colace-Sauty","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"N.","family":"Beaume","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H.","family":"Cartonnet","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J.","family":"Guegan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"D.","family":"Ulveling","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C.","family":"Pardanaud-Glavieux","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4238-1166","authenticated-orcid":false,"given":"I.","family":"Moszer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H.","family":"Cheval","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0393-9262","authenticated-orcid":false,"given":"P.","family":"Ravassard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,2,5]]},"reference":[{"key":"37872_CR1","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1007\/BF01248996","volume":"57","author":"DC German","year":"1983","unstructured":"German, D. C., Schlusselberg, D. S. & Woodward, D. J. Three-dimensional computer reconstruction of midbrain dopaminergic neuronal populations: from mouse to man. J Neural Transm 57, 243\u2013254 (1983).","journal-title":"J Neural Transm"},{"key":"37872_CR2","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1136\/jnnp.54.1.30","volume":"54","author":"B Pakkenberg","year":"1991","unstructured":"Pakkenberg, B., Moller, A., Gundersen, H. J., Mouritzen Dam, A. & Pakkenberg, H. The absolute number of nerve cells in substantia nigra in normal subjects and in patients with Parkinson\u2019s disease estimated with an unbiased stereological method. J Neurol Neurosurg Psychiatry 54, 30\u201333 (1991).","journal-title":"J Neurol Neurosurg Psychiatry"},{"key":"37872_CR3","doi-asserted-by":"publisher","first-page":"1150","DOI":"10.1016\/S1474-4422(09)70238-8","volume":"8","author":"DW Dickson","year":"2009","unstructured":"Dickson, D. W. et al. Neuropathological assessment of Parkinson\u2019s disease: refining the diagnostic criteria. Lancet Neurol 8, 1150\u20131157, https:\/\/doi.org\/10.1016\/S1474-4422(09)70238-8 (2009).","journal-title":"Lancet Neurol"},{"key":"37872_CR4","doi-asserted-by":"publisher","first-page":"896","DOI":"10.1016\/S0140-6736(14)61393-3","volume":"386","author":"LV Kalia","year":"2015","unstructured":"Kalia, L. V. & Lang, A. E. Parkinson\u2019s disease. Lancet 386, 896\u2013912, https:\/\/doi.org\/10.1016\/S0140-6736(14)61393-3 (2015).","journal-title":"Lancet"},{"key":"37872_CR5","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1038\/nrn.2016.165","volume":"18","author":"M Morales","year":"2017","unstructured":"Morales, M. & Margolis, E. B. Ventral tegmental area: cellular heterogeneity, connectivity and behaviour. Nat Rev Neurosci 18, 73\u201385, https:\/\/doi.org\/10.1038\/nrn.2016.165 (2017).","journal-title":"Nat Rev Neurosci"},{"key":"37872_CR6","doi-asserted-by":"publisher","first-page":"152","DOI":"10.3389\/fnana.2014.00152","volume":"8","author":"L Brichta","year":"2014","unstructured":"Brichta, L. & Greengard, P. Molecular determinants of selective dopaminergic vulnerability in Parkinson\u2019s disease: an update. Front Neuroanat 8, 152, https:\/\/doi.org\/10.3389\/fnana.2014.00152 (2014).","journal-title":"Front Neuroanat"},{"issue":"Pt 8","key":"37872_CR7","doi-asserted-by":"publisher","first-page":"1437","DOI":"10.1093\/brain\/122.8.1437","volume":"122","author":"P Damier","year":"1999","unstructured":"Damier, P., Hirsch, E. C., Agid, Y. & Graybiel, A. M. The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson\u2019s disease. Brain 122(Pt 8), 1437\u20131448 (1999).","journal-title":"Brain"},{"key":"37872_CR8","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1038\/334345a0","volume":"334","author":"E Hirsch","year":"1988","unstructured":"Hirsch, E., Graybiel, A. M. & Agid, Y. A. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson\u2019s disease. Nature 334, 345\u2013348, https:\/\/doi.org\/10.1038\/334345a0 (1988).","journal-title":"Nature"},{"key":"37872_CR9","doi-asserted-by":"publisher","first-page":"566","DOI":"10.1016\/j.cell.2016.09.027","volume":"167","author":"G La Manno","year":"2016","unstructured":"La Manno, G. et al. Molecular Diversity of Midbrain Development in Mouse, Human, and Stem Cells. Cell 167, 566\u2013580 e519, https:\/\/doi.org\/10.1016\/j.cell.2016.09.027 (2016).","journal-title":"Cell"},{"key":"37872_CR10","doi-asserted-by":"publisher","first-page":"930","DOI":"10.1016\/j.celrep.2014.10.008","volume":"9","author":"JF Poulin","year":"2014","unstructured":"Poulin, J. F. et al. Defining midbrain dopaminergic neuron diversity by single-cell gene expression profiling. Cell Rep 9, 930\u2013943, https:\/\/doi.org\/10.1016\/j.celrep.2014.10.008 (2014).","journal-title":"Cell Rep"},{"key":"37872_CR11","doi-asserted-by":"publisher","first-page":"336","DOI":"10.1016\/j.tins.2013.03.003","volume":"36","author":"J Roeper","year":"2013","unstructured":"Roeper, J. Dissecting the diversity of midbrain dopamine neurons. Trends Neurosci 36, 336\u2013342, https:\/\/doi.org\/10.1016\/j.tins.2013.03.003 (2013).","journal-title":"Trends Neurosci"},{"key":"37872_CR12","doi-asserted-by":"publisher","first-page":"59","DOI":"10.3389\/fnana.2017.00059","volume":"11","author":"MP Smidt","year":"2017","unstructured":"Smidt, M. P. Molecular Programming of Mesodiencephalic Dopaminergic Neuronal Subsets. Front Neuroanat 11, 59, https:\/\/doi.org\/10.3389\/fnana.2017.00059 (2017).","journal-title":"Front Neuroanat"},{"key":"37872_CR13","doi-asserted-by":"publisher","first-page":"1918","DOI":"10.1242\/dev.097394","volume":"142","author":"E Arenas","year":"2015","unstructured":"Arenas, E., Denham, M. & Villaescusa, J. C. How to make a midbrain dopaminergic neuron. Development 142, 1918\u20131936, https:\/\/doi.org\/10.1242\/dev.097394 (2015).","journal-title":"Development"},{"key":"37872_CR14","doi-asserted-by":"publisher","first-page":"661","DOI":"10.1242\/dev.099937","volume":"141","author":"GO Bodea","year":"2014","unstructured":"Bodea, G. O. et al. Reelin and CXCL12 regulate distinct migratory behaviors during the development of the dopaminergic system. Development 141, 661\u2013673, https:\/\/doi.org\/10.1242\/dev.099937 (2014).","journal-title":"Development"},{"key":"37872_CR15","doi-asserted-by":"publisher","first-page":"716","DOI":"10.1073\/pnas.0706729105","volume":"105","author":"TR Mercer","year":"2008","unstructured":"Mercer, T. R., Dinger, M. E., Sunkin, S. M., Mehler, M. F. & Mattick, J. S. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci USA 105, 716\u2013721, https:\/\/doi.org\/10.1073\/pnas.0706729105 (2008).","journal-title":"Proc Natl Acad Sci USA"},{"key":"37872_CR16","doi-asserted-by":"publisher","first-page":"1915","DOI":"10.1101\/gad.17446611","volume":"25","author":"MN Cabili","year":"2011","unstructured":"Cabili, M. N. et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25, 1915\u20131927, https:\/\/doi.org\/10.1101\/gad.17446611 (2011).","journal-title":"Genes Dev"},{"key":"37872_CR17","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1016\/j.cmet.2012.08.010","volume":"16","author":"I Moran","year":"2012","unstructured":"Moran, I. et al. Human beta cell transcriptome analysis uncovers lncRNAs that are tissue-specific, dynamically regulated, and abnormally expressed in type 2 diabetes. Cell Metab 16, 435\u2013448, https:\/\/doi.org\/10.1016\/j.cmet.2012.08.010 (2012).","journal-title":"Cell Metab"},{"key":"37872_CR18","doi-asserted-by":"publisher","first-page":"1168","DOI":"10.1038\/nn.4063","volume":"18","author":"P Yao","year":"2015","unstructured":"Yao, P. et al. Coexpression networks identify brain region-specific enhancer RNAs in the human brain. Nat Neurosci 18, 1168\u20131174, https:\/\/doi.org\/10.1038\/nn.4063 (2015).","journal-title":"Nat Neurosci"},{"key":"37872_CR19","doi-asserted-by":"publisher","first-page":"400","DOI":"10.1016\/j.cmet.2016.11.016","volume":"25","author":"I Akerman","year":"2017","unstructured":"Akerman, I. et al. Human Pancreatic beta Cell lncRNAs Control Cell-Specific Regulatory Networks. Cell Metab 25, 400\u2013411, https:\/\/doi.org\/10.1016\/j.cmet.2016.11.016 (2017).","journal-title":"Cell Metab"},{"key":"37872_CR20","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1038\/nrm3949","volume":"16","author":"S Heinz","year":"2015","unstructured":"Heinz, S., Romanoski, C. E., Benner, C. & Glass, C. K. The selection and function of cell type-specific enhancers. Nat Rev Mol Cell Biol 16, 144\u2013154, https:\/\/doi.org\/10.1038\/nrm3949 (2015).","journal-title":"Nat Rev Mol Cell Biol"},{"key":"37872_CR21","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1016\/j.cell.2010.09.001","volume":"143","author":"UA Orom","year":"2010","unstructured":"Orom, U. A. et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 143, 46\u201358, https:\/\/doi.org\/10.1016\/j.cell.2010.09.001 (2010).","journal-title":"Cell"},{"key":"37872_CR22","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/j.cell.2013.06.020","volume":"154","author":"I Ulitsky","year":"2013","unstructured":"Ulitsky, I. & Bartel, D. P. lincRNAs: genomics, evolution, and mechanisms. Cell 154, 26\u201346, https:\/\/doi.org\/10.1016\/j.cell.2013.06.020 (2013).","journal-title":"Cell"},{"key":"37872_CR23","doi-asserted-by":"publisher","first-page":"1097","DOI":"10.1016\/j.bbagrm.2014.08.012","volume":"1839","author":"G Yang","year":"2014","unstructured":"Yang, G., Lu, X. & Yuan, L. LncRNA: a link between RNA and cancer. Biochim Biophys Acta 1839, 1097\u20131109, https:\/\/doi.org\/10.1016\/j.bbagrm.2014.08.012 (2014).","journal-title":"Biochim Biophys Acta"},{"key":"37872_CR24","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/978-981-10-5203-3_1","volume":"1008","author":"J Jarroux","year":"2017","unstructured":"Jarroux, J., Morillon, A. & Pinskaya, M. History, Discovery, and Classification of lncRNAs. Adv Exp Med Biol 1008, 1\u201346, https:\/\/doi.org\/10.1007\/978-981-10-5203-3_1 (2017).","journal-title":"Adv Exp Med Biol"},{"key":"37872_CR25","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1016\/j.cub.2005.02.027","volume":"15","author":"TL Young","year":"2005","unstructured":"Young, T. L., Matsuda, T. & Cepko, C. L. The noncoding RNA taurine upregulated gene 1 is required for differentiation of the murine retina. Curr Biol 15, 501\u2013512, https:\/\/doi.org\/10.1016\/j.cub.2005.02.027 (2005).","journal-title":"Curr Biol"},{"key":"37872_CR26","doi-asserted-by":"publisher","first-page":"1020","DOI":"10.1038\/nn.2371","volume":"12","author":"AM Bond","year":"2009","unstructured":"Bond, A. M. et al. Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry. Nat Neurosci 12, 1020\u20131027, https:\/\/doi.org\/10.1038\/nn.2371 (2009).","journal-title":"Nat Neurosci"},{"key":"37872_CR27","doi-asserted-by":"publisher","first-page":"616","DOI":"10.1016\/j.stem.2013.03.003","volume":"12","author":"AD Ramos","year":"2013","unstructured":"Ramos, A. D. et al. Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. Cell Stem Cell 12, 616\u2013628, https:\/\/doi.org\/10.1016\/j.stem.2013.03.003 (2013).","journal-title":"Cell Stem Cell"},{"key":"37872_CR28","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1007\/978-981-10-5203-3_9","volume":"1008","author":"BS Clark","year":"2017","unstructured":"Clark, B. S. & Blackshaw, S. Understanding the Role of lncRNAs in Nervous System Development. Adv Exp Med Biol 1008, 253\u2013282, https:\/\/doi.org\/10.1007\/978-981-10-5203-3_9 (2017).","journal-title":"Adv Exp Med Biol"},{"key":"37872_CR29","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1126\/science.1156409","volume":"322","author":"D Altshuler","year":"2008","unstructured":"Altshuler, D., Daly, M. J. & Lander, E. S. Genetic mapping in human disease. Science 322, 881\u2013888, https:\/\/doi.org\/10.1126\/science.1156409 (2008).","journal-title":"Science"},{"key":"37872_CR30","doi-asserted-by":"publisher","first-page":"6046","DOI":"10.1093\/nar\/gkw500","volume":"44","author":"A Brodie","year":"2016","unstructured":"Brodie, A., Azaria, J. R. & Ofran, Y. How far from the SNP may the causative genes be? Nucleic Acids Res 44, 6046\u20136054, https:\/\/doi.org\/10.1093\/nar\/gkw500 (2016).","journal-title":"Nucleic Acids Res"},{"key":"37872_CR31","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.pneurobio.2017.03.004","volume":"156","author":"MJ Millan","year":"2017","unstructured":"Millan, M. J. Linking deregulation of non-coding RNA to the core pathophysiology of Alzheimer\u2019s disease: An integrative review. Prog Neurobiol 156, 1\u201368, https:\/\/doi.org\/10.1016\/j.pneurobio.2017.03.004 (2017).","journal-title":"Prog Neurobiol"},{"key":"37872_CR32","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1016\/j.bbrc.2016.11.143","volume":"485","author":"LK Wang","year":"2017","unstructured":"Wang, L. K., Chen, X. F., He, D. D., Li, Y. & Fu, J. Dissection of functional lncRNAs in Alzheimer\u2019s disease by construction and analysis of lncRNA-mRNA networks based on competitive endogenous RNAs. Biochem Biophys Res Commun 485, 569\u2013576, https:\/\/doi.org\/10.1016\/j.bbrc.2016.11.143 (2017).","journal-title":"Biochem Biophys Res Commun"},{"key":"37872_CR33","doi-asserted-by":"publisher","first-page":"114","DOI":"10.3389\/fncel.2015.00114","volume":"9","author":"C Carrieri","year":"2015","unstructured":"Carrieri, C. et al. Expression analysis of the long non-coding RNA antisense to Uchl1 (AS Uchl1) during dopaminergic cells\u2019 differentiation in vitro and in neurochemical models of Parkinson\u2019s disease. Front Cell Neurosci 9, 114, https:\/\/doi.org\/10.3389\/fncel.2015.00114 (2015).","journal-title":"Front Cell Neurosci"},{"key":"37872_CR34","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1038\/nature17939","volume":"533","author":"F Soldner","year":"2016","unstructured":"Soldner, F. et al. Parkinson-associated risk variant in distal enhancer of alpha-synuclein modulates target gene expression. Nature 533, 95\u201399, https:\/\/doi.org\/10.1038\/nature17939 (2016).","journal-title":"Nature"},{"key":"37872_CR35","doi-asserted-by":"publisher","first-page":"2869","DOI":"10.1007\/s12035-016-9854-x","volume":"54","author":"TFJ Kraus","year":"2017","unstructured":"Kraus, T. F. J. et al. Altered Long Noncoding RNA Expression Precedes the Course of Parkinson\u2019s Disease-a Preliminary Report. Mol Neurobiol 54, 2869\u20132877, https:\/\/doi.org\/10.1007\/s12035-016-9854-x (2017).","journal-title":"Mol Neurobiol"},{"key":"37872_CR36","doi-asserted-by":"publisher","first-page":"48","DOI":"10.3389\/fgene.2014.00048","volume":"5","author":"D Vucicevic","year":"2014","unstructured":"Vucicevic, D., Schrewe, H. & Orom, U. A. Molecular mechanisms of long ncRNAs in neurological disorders. Front Genet 5, 48, https:\/\/doi.org\/10.3389\/fgene.2014.00048 (2014).","journal-title":"Front Genet"},{"key":"37872_CR37","doi-asserted-by":"publisher","first-page":"71087","DOI":"10.18632\/oncotarget.12122","volume":"7","author":"J Hu","year":"2016","unstructured":"Hu, J. et al. Systematically characterizing dysfunctional long intergenic non-coding RNAs in multiple brain regions of major psychosis. Oncotarget 7, 71087\u201371098, https:\/\/doi.org\/10.18632\/oncotarget.12122 (2016).","journal-title":"Oncotarget"},{"key":"37872_CR38","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.pnpbp.2016.06.004","volume":"73","author":"X Huang","year":"2017","unstructured":"Huang, X., Luo, Y. L., Mao, Y. S. & Ji, J. L. The link between long noncoding RNAs and depression. Prog Neuropsychopharmacol Biol Psychiatry 73, 73\u201378, https:\/\/doi.org\/10.1016\/j.pnpbp.2016.06.004 (2017).","journal-title":"Prog Neuropsychopharmacol Biol Psychiatry"},{"key":"37872_CR39","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1111\/jnc.13255","volume":"135","author":"MJ Bannon","year":"2015","unstructured":"Bannon, M. J. et al. Identification of long noncoding RNAs dysregulated in the midbrain of human cocaine abusers. J Neurochem 135, 50\u201359, https:\/\/doi.org\/10.1111\/jnc.13255 (2015).","journal-title":"J Neurochem"},{"key":"37872_CR40","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1038\/ng.2870","volume":"46","author":"L Pasquali","year":"2014","unstructured":"Pasquali, L. et al. Pancreatic islet enhancer clusters enriched in type 2 diabetes risk-associated variants. Nat Genet 46, 136\u2013143, https:\/\/doi.org\/10.1038\/ng.2870 (2014).","journal-title":"Nat Genet"},{"key":"37872_CR41","doi-asserted-by":"publisher","first-page":"6423","DOI":"10.1073\/pnas.111152398","volume":"98","author":"K Sawamoto","year":"2001","unstructured":"Sawamoto, K. et al. Visualization, direct isolation, and transplantation of midbrain dopaminergic neurons. Proc Natl Acad Sci USA 98, 6423\u20136428, https:\/\/doi.org\/10.1073\/pnas.111152398 (2001).","journal-title":"Proc Natl Acad Sci USA"},{"key":"37872_CR42","doi-asserted-by":"publisher","first-page":"e74","DOI":"10.1093\/nar\/gkt006","volume":"41","author":"L Wang","year":"2013","unstructured":"Wang, L. et al. CPAT: Coding-Potential Assessment Tool using an alignment-free logistic regression model. Nucleic Acids Res 41, e74, https:\/\/doi.org\/10.1093\/nar\/gkt006 (2013).","journal-title":"Nucleic Acids Res"},{"key":"37872_CR43","doi-asserted-by":"publisher","first-page":"1775","DOI":"10.1101\/gr.132159.111","volume":"22","author":"T Derrien","year":"2012","unstructured":"Derrien, T. et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22, 1775\u20131789, https:\/\/doi.org\/10.1101\/gr.132159.111 (2012).","journal-title":"Genome Res"},{"key":"37872_CR44","doi-asserted-by":"publisher","first-page":"1055","DOI":"10.1021\/acschemneuro.5b00021","volume":"6","author":"V Niederkofler","year":"2015","unstructured":"Niederkofler, V., Asher, T. E. & Dymecki, S. M. Functional Interplay between Dopaminergic and Serotonergic Neuronal Systems during Development and Adulthood. ACS Chem Neurosci 6, 1055\u20131070, https:\/\/doi.org\/10.1021\/acschemneuro.5b00021 (2015).","journal-title":"ACS Chem Neurosci"},{"key":"37872_CR45","doi-asserted-by":"publisher","first-page":"293","DOI":"10.3389\/fncel.2016.00293","volume":"10","author":"J Grosch","year":"2016","unstructured":"Grosch, J., Winkler, J. & Kohl, Z. Early Degeneration of Both Dopaminergic and Serotonergic Axons - A Common Mechanism in Parkinson\u2019s Disease. Front Cell Neurosci 10, 293, https:\/\/doi.org\/10.3389\/fncel.2016.00293 (2016).","journal-title":"Front Cell Neurosci"},{"key":"37872_CR46","doi-asserted-by":"publisher","first-page":"4233","DOI":"10.1523\/JNEUROSCI.0126-07.2007","volume":"27","author":"CM Parras","year":"2007","unstructured":"Parras, C. M. et al. The proneural gene Mash1 specifies an early population of telencephalic oligodendrocytes. J Neurosci 27, 4233\u20134242, https:\/\/doi.org\/10.1523\/JNEUROSCI.0126-07.2007 (2007).","journal-title":"J Neurosci"},{"key":"37872_CR47","doi-asserted-by":"publisher","first-page":"2453","DOI":"10.1101\/gad.176008.111","volume":"25","author":"M Bergsland","year":"2011","unstructured":"Bergsland, M. et al. Sequentially acting Sox transcription factors in neural lineage development. Genes Dev 25, 2453\u20132464, https:\/\/doi.org\/10.1101\/gad.176008.111 (2011).","journal-title":"Genes Dev"},{"key":"37872_CR48","doi-asserted-by":"crossref","unstructured":"Cui, H. & Bulleit, R. F. Expression of the POU transcription factor Brn-5 is an early event in the terminal differentiation of CNS neurons. J Neurosci Res 52, 625\u2013632, 10.1002\/(SICI)1097-4547(19980615)52:6<625::AID-JNR1>3.0.CO;2-A (1998).","DOI":"10.1002\/(SICI)1097-4547(19980615)52:6<625::AID-JNR1>3.0.CO;2-A"},{"key":"37872_CR49","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1016\/j.jgg.2016.05.002","volume":"43","author":"L Zhang","year":"2016","unstructured":"Zhang, L. et al. Targeted methylation sequencing reveals dysregulated Wnt signaling in Parkinson disease. J Genet Genomics 43, 587\u2013592, https:\/\/doi.org\/10.1016\/j.jgg.2016.05.002 (2016).","journal-title":"J Genet Genomics"},{"key":"37872_CR50","doi-asserted-by":"publisher","first-page":"2591","DOI":"10.1002\/cne.23051","volume":"520","author":"S Reyes","year":"2012","unstructured":"Reyes, S. et al. GIRK2 expression in dopamine neurons of the substantia nigra and ventral tegmental area. J Comp Neurol 520, 2591\u20132607, https:\/\/doi.org\/10.1002\/cne.23051 (2012).","journal-title":"J Comp Neurol"},{"key":"37872_CR51","doi-asserted-by":"publisher","unstructured":"Sun, Y. et al. The long noncoding RNA SNHG1 promotes tumor growth through regulating transcription of both local and distal genes. Oncogene, https:\/\/doi.org\/10.1038\/onc.2017.286 (2017).","DOI":"10.1038\/onc.2017.286"},{"key":"37872_CR52","doi-asserted-by":"publisher","first-page":"12041","DOI":"10.18632\/oncotarget.14510","volume":"8","author":"C Xu","year":"2017","unstructured":"Xu, C. et al. Systemically identifying and prioritizing risk lncRNAs through integration of pan-cancer phenotype associations. Oncotarget 8, 12041\u201312051, https:\/\/doi.org\/10.18632\/oncotarget.14510 (2017).","journal-title":"Oncotarget"},{"key":"37872_CR53","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.biopha.2016.02.036","volume":"80","author":"M Zhang","year":"2016","unstructured":"Zhang, M. et al. Long noncoding RNA SNHG1 predicts a poor prognosis and promotes hepatocellular carcinoma tumorigenesis. Biomed Pharmacother 80, 73\u201379, https:\/\/doi.org\/10.1016\/j.biopha.2016.02.036 (2016).","journal-title":"Biomed Pharmacother"},{"key":"37872_CR54","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1038\/nrg.2016.85","volume":"17","author":"I Ulitsky","year":"2016","unstructured":"Ulitsky, I. Evolution to the rescue: using comparative genomics to understand long non-coding RNAs. Nat Rev Genet 17, 601\u2013614, https:\/\/doi.org\/10.1038\/nrg.2016.85 (2016).","journal-title":"Nat Rev Genet"},{"key":"37872_CR55","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-15-845","volume":"15","author":"K Zhang","year":"2014","unstructured":"Zhang, K., Huang, K., Luo, Y. & Li, S. Identification and functional analysis of long non-coding RNAs in mouse cleavage stage embryonic development based on single cell transcriptome data. BMC Genomics 15, 845, https:\/\/doi.org\/10.1186\/1471-2164-15-845 (2014).","journal-title":"BMC Genomics"},{"key":"37872_CR56","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1016\/j.molmet.2016.01.002","volume":"5","author":"AM Ackermann","year":"2016","unstructured":"Ackermann, A. M., Wang, Z., Schug, J., Naji, A. & Kaestner, K. H. Integration of ATAC-seq and RNA-seq identifies human alpha cell and beta cell signature genes. Mol Metab 5, 233\u2013244, https:\/\/doi.org\/10.1016\/j.molmet.2016.01.002 (2016).","journal-title":"Mol Metab"},{"key":"37872_CR57","doi-asserted-by":"publisher","first-page":"989","DOI":"10.1038\/ng.3043","volume":"46","author":"MA Nalls","year":"2014","unstructured":"Nalls, M. A. et al. Large-scale meta-analysis of genome-wide association data identifies six new risk loci for Parkinson\u2019s disease. Nat Genet 46, 989\u2013993, https:\/\/doi.org\/10.1038\/ng.3043 (2014).","journal-title":"Nat Genet"},{"key":"37872_CR58","doi-asserted-by":"publisher","first-page":"1511","DOI":"10.1038\/ng.3955","volume":"49","author":"D Chang","year":"2017","unstructured":"Chang, D. et al. A meta-analysis of genome-wide association studies identifies 17 new Parkinson\u2019s disease risk loci. Nat Genet 49, 1511\u20131516, https:\/\/doi.org\/10.1038\/ng.3955 (2017).","journal-title":"Nat Genet"},{"key":"37872_CR59","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2013-14-4-r36","volume":"14","author":"D Kim","year":"2013","unstructured":"Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14, R36, https:\/\/doi.org\/10.1186\/gb-2013-14-4-r36 (2013).","journal-title":"Genome Biol"},{"key":"37872_CR60","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2105-14-128","volume":"14","author":"EY Chen","year":"2013","unstructured":"Chen, E. Y. et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14, 128, https:\/\/doi.org\/10.1186\/1471-2105-14-128 (2013).","journal-title":"BMC Bioinformatics"},{"key":"37872_CR61","doi-asserted-by":"publisher","first-page":"W90","DOI":"10.1093\/nar\/gkw377","volume":"44","author":"MV Kuleshov","year":"2016","unstructured":"Kuleshov, M. V. et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res 44, W90\u201397, https:\/\/doi.org\/10.1093\/nar\/gkw377 (2016).","journal-title":"Nucleic Acids Res"},{"key":"37872_CR62","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1038\/nbt.1630","volume":"28","author":"CY McLean","year":"2010","unstructured":"McLean, C. Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 28, 495\u2013501, https:\/\/doi.org\/10.1038\/nbt.1630 (2010).","journal-title":"Nat Biotechnol"},{"key":"37872_CR63","doi-asserted-by":"publisher","first-page":"W50","DOI":"10.1093\/nar\/gkv362","volume":"43","author":"A Medina-Rivera","year":"2015","unstructured":"Medina-Rivera, A. et al. RSAT 2015: Regulatory Sequence Analysis Tools. Nucleic Acids Res 43, W50\u201356, https:\/\/doi.org\/10.1093\/nar\/gkv362 (2015).","journal-title":"Nucleic Acids Res"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-37872-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-37872-1","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-37872-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,17]],"date-time":"2022-12-17T05:25:56Z","timestamp":1671254756000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-37872-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,2,5]]},"references-count":63,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["37872"],"URL":"https:\/\/doi.org\/10.1038\/s41598-018-37872-1","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,2,5]]},"assertion":[{"value":"7 February 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 December 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 February 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"1409"}}