Long Noncoding RNA Expression Profiling During the Neuronal Differentiation of Glial Precursor Cells from Rat Dorsal Root Ganglia


Long noncoding RNAs (lncRNAs) play important roles in the process of cell fate determination. However, their function and expression profiles have not yet been systematically investigated during the transdifferentiation of glial precursor cells derived from dorsal root ganglia (DRG) in the peripheral nervous system. Our results demonstrated significant differences in gene architecture and expression among the three transcript types (lncRNA, mRNA, and TUCP). Distinct differences in transcript length, exon number, and ORF length were identified between lncRNAs and mRNAs after comparative analysis of their structure and sequence conservation. We found that the upregulated lncRNAs outnumbered the downregulated lncRNAs in glial precursor cells cultured with proBDNF antiserum compared with the levels in glial precursor cells cultured without proBDNF antiserum. By a series of GO and KEGG analyses, we found that the effects of some lncRNAs on their target genes in cis were related to nerve growth factor-induced cell cycle, cell phenotype change, and neuronal differentiation. The qRT-PCR verification results of lncRNAs ENSRNOT00000091991, ENSRNOT00000087717, and LNC000429 were mostly consistent with the sequencing results. The candidate lncRNAs may be associated with the neuronal transdifferentiation of glial precursor cells. Our study provides the first evidence for a remarkably diverse pattern of lncRNA expression during neuronal differentiation of glial precursor cells from rat DRG and also provides a resource for lncRNA studies in the field of cell differentiation.

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long noncoding RNA


dorsal root ganglia


intergenic lncRNA


long intergenic ncRNA


substance P


short hairpin RNA


poly D-lysine hydrobromide


glutamine synthetase


phosphate-buffered saline

Tuj 1:

neuron-specific class III beta-rubulin


calcitonin gene-related peptide


the fragments per kilobase of transcript per million fragments mapped


Coding-Noncoding Index


Coding Potential Calculator


open reading frame


Gene Ontology


Kyoto Encyclopedia of Genes and Genomes


protein-protein interactions


quantitative real time-polymerase chain reaction


precursor brain-derived neurotrophic factor




transcript of uncertain coding potential


phosphatidylinositol 3-kinase


  1. 1.

    Vierbuchen, T., A. Ostermeier, Z. P. Pang, Y. Kokubu, T. C. Südhof, and M. Wernig, (2010) Direct conversion of fibroblasts to functional neurons by denned factors. Nature. 463: 1035–1041.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Caiazzo, M., M. T. Dell’Anno, E. Dvoretskova, D. Lazarevic, S. Taverna, D. Leo, T. D. Sotnikova, A. Menegon, P. Roncaglia, G. Colciago, G. Russo, P. Carninci, G. Pezzoli, R. R. Gainetdinov, S. Gustincich, A. Dityatev, and V. Broccoli, (2011) Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature. 476: 224–227.

    CAS  PubMed  Google Scholar 

  3. 3.

    Pang, Z. P., N. Yang, T. Vierbuchen, A. Ostermeier, D. R. Fuentes, T. Q. Yang, A. Citri, V. Sebastiano, S. Marro, T. C. Südhof, and M. Wernig, (2011) Induction of human neuronal cells by defined transcription factors. Nature. 476: 220–223.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Pfisterer, U., A. Kirkeby, O. Torper, J. Wood, J. Nelander, A. Dufour, A. Björklund, O. Lindvall, J. Jakobsson, and M. Parmar, (2011) Direct conversion of human fibroblasts to dopaminergic neurons. Proc. Natl. Acad. Sci. USA. 108: 10343–10348.

    CAS  PubMed  Google Scholar 

  5. 5.

    Yoo, A. S., A. X. Sun, L. Li, A. Shcheglovitov, T. Portmann, Y. Li, C. Lee-Messer, R. E. Dolmetsch, R. W. Tsien, and G. R. Crabtree, (2011) MicroRNA-mediated conversion of human fibroblasts to neurons. Nature. 476: 228–231.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Efe, J. A., S. Hilcove, J. Kim, H. Zhou, K. Ouyang, G. Wang, J. Chen, and S. Ding, (2011) Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat. Cell Biol. 13: 215–222.

    CAS  PubMed  Google Scholar 

  7. 7.

    Huang, P., Z. He, S. Ji, H. Sun, D. Xiang, C. Liu, Y. Hu, X. Wang, and L. Hui, (2011) Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors. Nature. 475: 386–389.

    CAS  PubMed  Google Scholar 

  8. 8.

    Szabo, E., S. Rampalli, R. M. Risueno, A. Schnerch, R. Mitchell, A. Fiebig-Comyn, M. Levadoux-Martin, and M. Bhatia, (2010) Direct conversion of human fibroblasts to multilineage blood progenitors. Nature. 468: 521–526.

    CAS  PubMed  Google Scholar 

  9. 9.

    Kim, J., J. A. Efe, S. Zhu, M. Talantova, X. Yuan, S. Wang, S. A. Lipton, K. Zhang, and S. Ding, (2011) Direct reprogramming of mouse fibroblasts to neural progenitors. Proc. Natl. Acad. Sci. USA. 108: 7838–7843.

    CAS  PubMed  Google Scholar 

  10. 10.

    Lujan, E., S. Chanda, H. Ahlenius, T. C. Südhof, and M. Wernig, (2012) Direct conversion of mouse fibroblasts to self-renewing, tripotent neural precursor cells. Proc. Natl. Acad. Sci. USA. 109: 2527–2532.

    CAS  PubMed  Google Scholar 

  11. 11.

    Hanani, M., T. Y. Huang, P. S. Cherkas, M. Ledda, and E. Pannese, (2002) Glial cell plasticity in sensory ganglia induced by nerve damage. Neuroscience. 114: 279–283.

    CAS  PubMed  Google Scholar 

  12. 12.

    Soares, H. D., S. C. Chen, and J. I. Morgan, (2011) Differential and prolonged expression of Fos-lacZ and Jun-lacZ in neurons, glia, and muscle following sciatic nerve damage. Exp. Neurol. 167: 1–14.

    Google Scholar 

  13. 13.

    Zhou, X. E, R. A. Rush, and E. M. Mclachlan, (1996) Differential expression of the p75 nerve growth factor receptor in glia and neurons of the rat dorsal root ganglia after peripheral nerve transection. J. Neurosci. 16: 2901–2911.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Li, H. Y., E. H. M. Say, and X. F. Zhou, (2007) Isolation and characterization of neural crest progenitors from adult dorsal root ganglia. Stem Cells. 25: 2053–2065.

    CAS  PubMed  Google Scholar 

  15. 15.

    Fex Svenningsen, A., D. R. Colman, and L. Pedraza, (2004) Satellite cells of dorsal root ganglia are multipotential glial precursors. Neuron. Glia Biol. 1: 85–93.

    PubMed  Google Scholar 

  16. 16.

    Kim, J. B., V. Sebastiano, G. Wu, M. J. Araúzo-Bravo, P. Sasse, L. Gentile, K. Ko, D. Ruau, M. Ehrich, D. van den Boom, J. Meyer, K. Hübner, C. Bernemann, C. Ortmeier, M. Zenke, B. K. Fleischmann, H. Zaehres, and H. R. Schöler (2009) Oct4-induced pluripotency in adult neural stem cells. Cell. 136: 411–419.

    CAS  PubMed  Google Scholar 

  17. 17.

    Deleidi, M., O. Cooper, G. Hargus, A. Levy, and O. Isacson, (2011) Oct4-induced reprogramming is required for adult brain neural stem cell differentiation into midbrain dopaminergic neurons. PLoS One. 6: el 9926.

    Google Scholar 

  18. 18.

    Mitchell, R, E. Szabo, Z. Shapovalova, L. Aslostovar, K. Makondo, and M. Bhatia, (2014) Molecular evidence for OCT4-induced plasticity in adult human fibroblasts required for direct cell fate conversion to lineage specific progenitors. Stem Cells. 32: 2178–2187.

    CAS  PubMed  Google Scholar 

  19. 19.

    Chanda, S., C. E. Ang, J. Davila, C. Pak, M. Mall, Q. Y. Lee, H. Ahlenius, S. W. Jung, T. C. Südhof, and M. Wernig, (2014) Generation of induced neuronal cells by the single reprogramming factor ASCL1. Stem Cell Reports. 3: 282–296.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Knauss, J. L. and T. Sun, (2013) Regulatory mechanisms of long noncoding RNAs in vertebrate central nervous system development and function. Neuroscience. 235: 200–214.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Johnson, R. (2012) Long non-coding RNAs in Huntington’s disease neurodegeneration. Neurobiol. Dis. 46: 245–254.

    CAS  PubMed  Google Scholar 

  22. 22.

    Qureshi, I. A., J. S. Mattick, and M. F. Mehler, (2010) Long non-coding RNAs in nervous system function and disease. Brain Res. 1338: 20–35.

    CAS  PubMed  Google Scholar 

  23. 23.

    Kiryuseo, S. and H. Kiyama, (2011) The nuclear events guiding successful nerve regeneration. Front. Mol. Neurosci. 4: 53.

    Google Scholar 

  24. 24.

    Jiang, B. C, W. X. Sun, L. N. He, D. L. Cao, Z. J. Zhang, and Y. J. Gao, (2015) Identification of lncRNA expression profile in the spinal cord of mice following spinal nerve ligation-induced neuropathic pain. Mol. Pain. 11: 43.

    PubMed  PubMed Central  Google Scholar 

  25. 25.

    Peng, H., L. Zou, J. Xie, H. Wu, B. Wu, G. Zhu, Q. Lv, X. Zhang, S. Liu, G. Li, H. Xu, Y. Gao, C. Xu, C. Zhang, S. Wang, Y. Xue, and S. Liang, (2016) lncRNA NONRATT021972 siRNA decreases diabetic neuropathic pain mediated by the P2X3 receptor in dorsal root ganglia. Mol. Neurobiol. 54: 511–523.

    PubMed  Google Scholar 

  26. 26.

    Zou, L., G. Tu, W. Xie, S. Wen, Q. Xie, S. Liu, G. Li, Y. Gao, H. Xu, S. Wang, Y. Xue, B. Wu, Q. Lv, M. Ying, X. Zhang, and S. Liang, (2016) LncRNA NONRATT021972 involved the pathophysiologic processes mediated by P2X7 receptors in stellate ganglia after myocardial ischemic injury. Purinergic Signal. 12: 127–137.

    CAS  PubMed  Google Scholar 

  27. 27.

    Zhou, J., Q. Xiong, H. Chen, C. Yang, and Y. Fan, (2017) Identification of the spinal expression profile of non-coding RNAs involved in neuropathic pain following spared nerve injury by sequence analysis. Front. Mol. Neurosci. 10: 91.

    PubMed  PubMed Central  Google Scholar 

  28. 28.

    Wang, S., H. Xu, L. Zou, J. Xie, H. Wu, B. Wu, Z. Yi, Q. Lv, X. Zhang, M. Ying, S. Liu, G. Li, Y. Gao, C. Xu, C. Zhang, Y. Xue, and S. Liang, (2016) LncRNA uc.48+ is involved in diabetic neuropathic pain mediated by the P2X3 receptor in the dorsal root ganglia. Purinergic Signal. 12: 139–148.

    CAS  PubMed  Google Scholar 

  29. 29.

    Mehler, M. F. and J. S. Mattick, (2007) Noncoding RNAs and RNA editing in brain development, functional diversification, and neurological disease. Physiol. Rev. 87: 799–823.

    CAS  PubMed  Google Scholar 

  30. 30.

    Mehler, M. F. and J. S. Mattick, (2006) Non-coding RNAs in the nervous system. J. Physiol. 575: 333–341.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Mercer, T. R, M. E. Dinger, S. M. Sunkin, M. F. Mehler, and J. S. Mattick, (2008) Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl. Acad. Sci. USA. 105: 716–721.

    CAS  PubMed  Google Scholar 

  32. 32.

    Dinger, M. E., P. P. Amaral, T. R. Mercer, K. C. Pang, S. J. Bruce, B. B. Gardiner, M. E. Askarian-Amiri, K. Ru, G. Soldà, C. Simons, S. M. Sunkin, M. L. Crowe, S. M. Grimmond, A. C. Perkins, and J. S. Mattick, (2008) Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 18: 1433–1445.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Pang, K. C., M. E. Dinger, T. R. Mercer, L. Malquori, S. M. Grimmond, W. Chen, and J. S. Mattick, (2009) Genome-wide identification of long noncoding RNAs in CD8+ T cells. J. Immunol. 182: 7738–7748.

    CAS  PubMed  Google Scholar 

  34. 34.

    Guttman, M., J. Donaghey, B. W. Carey, M. Garber, J. K. Grenier, G. Munson, G. Young, A. B. Lucas, R. Ach, L. Bruhn, X. Yang, I. Amit, A. Meissner, A. Regev, J. L. Rinn, D. E. Root, and E. S. Lander, (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature. 477: 295–300.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Mercer, T. R., I. A. Qureshi, S. Gokhan, M. E. Dinger, G. Li, J. S. Mattick, and M. F. Mehler, (2010) Long noncoding RNAs in neuronal-glial fate specification and oligodendrocyte lineage maturation. BMC Neurosci. 11: 14.

    PubMed  PubMed Central  Google Scholar 

  36. 36.

    Mingyan, L., E. Pedrosa, A. Shah, A. Hrabovsky, S. Maqbool, D. Zheng, and H. M. Lachman, (2011) RNA-Seq of human neurons derived from iPS cells reveals candidate long non-coding RNAs involved in neurogenesis and neuropsychiatrie disorders. PLoS One. 6: e23356.

    Google Scholar 

  37. 37.

    Ng, S. Y, R. Johnson, and L. W. Stanton, (2012) Human long noncoding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors. EMBO J. 31:522–533.

    CAS  PubMed  Google Scholar 

  38. 38.

    Trapnell, C, B. A. Williams, G. Pertea, A. Mortazavi, G. Kwan, M. J. van Baren, S. L. Salzberg, B. J. Wold, and L. Pachter, (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28: 511–515.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Sun, L., H. Luo, D. Bu, G. Zhao, K. Yu, C. Zhang, Y. Liu, R. Chen, and Y. Zhao, (2013) Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts. Nucleic Acids Res. 41: e166.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Kong, L., Y. Zhang, Z. Q. Ye, X. Q. Liu, S. Q. Zhao, L. Wei, and G. Gao, (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res. 35: W345–W349.

    PubMed  PubMed Central  Google Scholar 

  41. 41.

    Punta, M., P. C. Coggill, R. Y. Eberhardt, J. Misty, J. Tate, C. Boursnell, N. Pang, K. Forslund, G. Ceric, J. Clements, A. Heger, L. Holm, E. L. L. Sonnhammer, S. R. Eddy, A. Bateman, and R. D. Finn, (2012) The Pfam protein families database. Nucleic Acids Res. 40: D290–D301.

    CAS  PubMed  Google Scholar 

  42. 42.

    Trapnell, C, A. Roberts, L. Goff, G. Pertea, D. Kim, D. R. Kelley, H. Pimentel, S. L. Salzberg, J. L. Rinn, and L. Pachter, (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7: 562–578.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Orom, U. A., T. Derrien, M. Beringer, K. Gumireddy, A. Gardini, G. Bussotti, F. Lai, M. Zytnicki, C. Notredame, Q. Huang, R. Guigo, and R. Shiekhattar, (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell. 143: 46–58.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Ren, H., G. Wang, L. Chen, J. Jiang, L. Liu, N. Li, J. Zhao, X. Sun, and P. Zhou, (2016) Genome-wide analysis of long non-coding RNAs at early stage of skin pigmentation in goats (Copra hircus). BMC Genomics. 17: 67.

    PubMed  PubMed Central  Google Scholar 

  45. 45.

    Langfelder, P. and S. Horvath, (2008) WGCNA: an Rpackage for weighted correlation network analysis. BMC Bioinformatics. 9: 559.

    PubMed  PubMed Central  Google Scholar 

  46. 46.

    Miyamoto, K., H. Yamakawa, N. Muraoka, T. Sadahiro, T. Umei, M. Isomi, H. Nakasima, M. Akiyama, K. Fukuda, and M. Ieda, (2014) Direct reprogramming of fibroblasts into functional cardiomyocyte-like cells without viral integration. J. Card. Fail. 20: S145.

    Google Scholar 

  47. 47.

    Marro, S. and N. Yang, (2014) Transdifferentiation of mouse fibroblasts and hepatocytes to functional neurons. Methods Mol. Biol. 1150: 237–246.

    CAS  PubMed  Google Scholar 

  48. 48.

    Ulrich, P., J. Wood, K. Nihlberg, O. Hallgren, L. Bjermer, G. Westergren-Thorsson, O. Lindvall, and M. Parmar, (2011) Efficient induction of functional neurons from adult human fibroblasts. Cell Cycle. 10:3311–3316.

    Google Scholar 

  49. 49.

    George, D., P. Ahrens, and S. Lambert, (2018) Satellite glial cells represent a population of developmentally arrested Schwann cells. Glia. 66: 1496–1506.

    PubMed  Google Scholar 

  50. 50.

    Gomes, C. P., S. Nóbrega-Pereira, B. Domingues-Silva, K. Rebelo, C. Alves-Vale, S. P. Marinho, T. Carvalho, S. Dias, and B. Bernardes de Jesus (2019) An antisense transcript mediates MALATl response in human breast cancer. BMC Cancer. 19: 771.

    PubMed  PubMed Central  Google Scholar 

  51. 51.

    Faghihi, M. A. and C. Wahlestedt, (2009) Regulatory roles of natural antisense transcripts. Nat. Rev. Mol. Cell Biol. 10: 637–643.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Canzio, D., C. L. Nwakeze, A. Horta, S. M. Rajkumar, E. L. Coffey, E. E. Duffy, R. Duffié, K. Monahan, S. O’Keeffe, M. D. Simon, S. Lomvardas, and T. Maniatis, (2019) Antisense lncRNA transcription mediates DNA demethylation to drive stochastic protocadherin a promoter choice. Cell. 177: 639–653.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Cabili, M. N., C. Trapnell, L. Goff, M. Koziol, B. Tazon-Vega, A. Regev, and J. L. Rinn, (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 25: 1915–1927.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Guttman, M., I. Amit, M. Garber, C. French, M. F. Lin, D. Feldser, M. Huarte, O. Zuk, B. W. Carey, J. P. Cassady, M. N. Cabili, R. Jaenisch, T. S. Mikkelsen, T. Jacks, N. Hacohen, B. E. Bernstein, M. Kellis, A. Regev, J. L. Rinn, and E. S. Lander, (2009) Chromatin signature reveals over a thousand highly conserved large non-coding Rnas in mammals. Nature. 458: 223–227.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Rodova, M., A. N. Nguyen, and G. Blanco, (2006) The transcription factor CREMtau and cAMP regulate promoter activity of the Na,K-ATPase alpha4 isoform. Mol. Reprod. Dev. 73: 1435–1447.

    CAS  PubMed  Google Scholar 

  56. 56.

    Ulitsky, I., A. Shkumatava, C. H. Jan, H. Sive, and D. P. Bartel, (2012) Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell. 147: 1537–1550.

    Google Scholar 

  57. 57.

    Nitsche, A., D. Rose, M. Fasold, K. Reiche, and P. F. Stadler, (2015) Comparison of splice sites reveals that long noncoding RNAs are evolutionarily well conserved. RNA. 21: 801–812.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Degen, M., F. Brellier, R. Kain, C. Ruiz, L. Terracciano, G. Orend, and R. Chiquet-Ehrismann (2007) Tenascin-W is a novel marker for activated tumor stroma in low-grade human breast cancer and influences cell behavior. Cancer Res. 67: 9169–9179.

    CAS  PubMed  Google Scholar 

  59. 59.

    Neidhardt, J., S. Fehr, M. Kutsche, J. Löhler, and M. Schachner, (2003) Tenascin-N: characterization of a novel member of the tenascin family that mediates neurite repulsion from hippocampal explants. Mol. Cell Neurosci. 23: 193–209.

    CAS  PubMed  Google Scholar 

  60. 60.

    Evilä, A., M. Arumilli, B. Udd, and P. Hackman, (2016) Targeted next-generation sequencing assay for detection of mutations in primary myopathies. Neuromuscul. Disord. 26: 7–15.

    PubMed  Google Scholar 

  61. 61.

    Nabieva, E., K. Jim, A. Agarwal, B. Chazelle, and M. Singh, (2005) Whole-proteome prediction of protein function via graph-theoretic analysis of interaction maps. Bioinformatics. 21 Suppl 1: 1302–1310.

    Google Scholar 

  62. 62.

    Lee, I., U. M. Blom, P. I. Wang, J. E. Shim, and E. M. Marcotte, (2011) Prioritizing candidate disease genes by network-based boosting of genome-wide association data. Genome Res. 21: 1109–1121.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Kovâcs, I. A., K. Luck, K. Spirohn, Y. Wang, C. Pollis, S. Schlabach, W. Bian, D. K. Kim, N. Kishore, T. Hao, M. A. Calderwood, M. Vidal, and A. L. Barabâsi (2019) Network-based prediction of protein interactions. Nat Commun. 10: 1240.

    PubMed  PubMed Central  Google Scholar 

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We thank Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.


This work was supported by the National Natural Science Foundation of China (No. 31560295, to L.Y.L.); Yunnan Applied Basic Research Projects [No. 2018FE001(-163), to L.Y.L.; 2018FE001(-016), to W.M.]; Major Scientific and Technological Achievements Cultivation Projects of Kunming Medical University (CGPY201802, to L.Y.L.); and Research Innovation Team of Yunnan Province (2019HC022).

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L.Y.L. and J.H.G designed the study, and provided the funds and financial support for this research. Y.F.D., W.M., T.Z., J.W.Y, C.H.Z., K.P.L., X.B.W., J.W.W., Z.W., X.K.Z., C.Y.L, J.J..L., and X.P.W. carried out the experimental study and analyzed the data. Y.F.D., W.M., and T.Z. wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Jianhui Guo or Liyan Li.

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Table S1. Glial cell culture medium

Table S2. The primer sequence information

Table S3. Gene structure and expression analysis of annotated lncRNA

Table S4. Gene structure and expression analysis of novel lncRNA

Table S5. Gene structure and expression analysis of mRNA

Table S6. The expression levels of lncRNA transcripts

Table S7. The expression levels of TUCP transcripts

Table S8. The expression levels of mRNA transcripts

Table S9. lncRNA target gene enrichment analysis in cis form

Table S10. KEGG pathways analysis of the proB12h vs. control group in cis form

Table S11. KEGG pathways analysis of the proB24h vs. control group in cis form

Table S12. KEGG pathways analysis of the proB3d vs. control group in cis form

Table S13. KEGG pathways analysis of the proB7d vs. control group in cis form

Table S14. KEGG pathways analysis of the proB12h vs. control group in trans form

Table S15. KEGG pathways analysis of the proB24h vs. control group in trans form

Table S16. KEGG pathways analysis of the proB3d vs. control group in trans form

Table S17. KEGG pathways analysis of the proB7d vs. control group in trans form

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Dai, Y., Ma, W., Zhang, T. et al. Long Noncoding RNA Expression Profiling During the Neuronal Differentiation of Glial Precursor Cells from Rat Dorsal Root Ganglia. Biotechnol Bioproc E 25, 356–373 (2020). https://doi.org/10.1007/s12257-019-0317-x

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  • lncRNA
  • mRNA
  • expression profiling
  • glial precursor cell
  • differentiation
  • proBDNF