Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Reviews in the Neurosciences

Editor-in-Chief: Huston, Joseph P.

Editorial Board Member: Topic, Bianca / Adeli, Hojjat / Buzsaki, Gyorgy / Crawley, Jacqueline / Crow, Tim / Eichenbaum, Howard / Gold, Paul / Holsboer, Florian / Korth, Carsten / Lubec, Gert / McEwen, Bruce / Pan, Weihong / Pletnikov, Mikhail / Robbins, Trevor / Schnitzler, Alfons / Stevens, Charles / Steward, Oswald / Trojanowski, John

8 Issues per year


IMPACT FACTOR 2016: 2.546
5-year IMPACT FACTOR: 3.191

CiteScore 2016: 3.30

SCImago Journal Rank (SJR) 2016: 1.249
Source Normalized Impact per Paper (SNIP) 2016: 0.983

Online
ISSN
2191-0200
See all formats and pricing
More options …
Volume 27, Issue 5 (Jul 2016)

Issues

Regulation of neuronal-glial fate specification by long non-coding RNAs

Lei Wang
  • Department of Neurosurgery, Affiliated Haikou Hospital, Xiangya School of Central South University, Haikou 570100, China
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Yan Liu / Shaiqi Sun
  • Department of Neurosurgery, Affiliated Haikou Hospital, Xiangya School of Central South University, Haikou 570100, China
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Ming Lu
  • Corresponding author
  • Department of Neurosurgery, the Second Affiliated Hospital of Hunan Normal University (PLA 163 Hospital), Cangsha 41000, China
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Ying Xia
  • Corresponding author
  • Department of Neurosurgery, Affiliated Haikou Hospital, Xiangya School of Central South University, Haikou 570100, China
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2016-03-04 | DOI: https://doi.org/10.1515/revneuro-2015-0061

Abstract

Neural stem cell transplantation is becoming a promising and attractive cell-based treatment modality for repairing the damaged central nervous system. One of the limitations of this approach is that the proportion of functional cells differentiated from stem cells still remains at a low level. In recent years, novel long non-coding RNAs (lncRNAs) are being discovered at a growing pace, suggesting that this class of molecules may act as novel regulators in neuronal-glial fate specification. In this review, we first describe the general features of lncRNAs that are more likely to be relevant to reveal their function. By this, we aim to point out the specific roles of a number of lncRNAs whose function has been described during neuronal and glial cell differentiation. There is no doubt that investigation of the lncRNAs will open a new window in studying neuronal-glial fate specification.

Keywords: differentiation; gliogenesis; lncRNAs; neurogenesis

References

  • Amaral, P.P. and Mattick, J.S. (2008). Noncoding RNA in development. Mammal. Genome 19, 454–492.Google Scholar

  • Amaral, P.P., Neyt, C., Wilkins, S.J., Askarian-Amiri, M.E., Sunkin, S.M., Perkins, A.C., and Mattick, J.S. (2009). Complex architecture and regulated expression of the Sox2ot locus during vertebrate development. RNA 15, 2013–2027.Google Scholar

  • Antoniou, D., Stergiopoulos, A., and Politis, P.K. (2014). Recent advances in the involvement of long non-coding RNAs in neural stem cell biology and brain pathophysiology. Front. Physiol. 5, 155.Google Scholar

  • Aprea, J. and Calegari, F. (2015). Long non-coding RNAs in corticogenesis: deciphering the non-coding code of the brain. EMBO J. 34, 2865–2884.Google Scholar

  • Barry, G., Briggs, J.A., Vanichkina, D.P., Poth, E.M., Beveridge, N.J., Ratnu, V.S., Nayler, S.P., Nones, K., Hu, J., Bredy, T.W., et al. (2014). The long non-coding RNA Gomafu is acutely regulated in response to neuronal activation and involved in schizophrenia-associated alternative splicing. Mol. Psychiatry 19, 486–494.Google Scholar

  • Bassett, A.R., Akhtar, A., Barlow, D.P., Bird, A.P., Brockdorff, N., Duboule, D., Ephrussi, A., Ferguson-Smith, A.C., Gingeras, T.R., Haerty, W., et al. (2014). Considerations when investigating lncRNA function in vivo. eLife 3, 1023–1033.Google Scholar

  • Batista, P.J. and Chang, H.Y. (2013). Long noncoding RNAs: cellular address codes in development and disease. Cell 152, 1298–1307.Google Scholar

  • Bernard, D., Prasanth, K.V., Tripathi, V., Colasse, S., Nakamura, T., Xuan, Z., Zhang, M.Q., Sedel, F., Jourdren, L., Coulpier, F., et al. (2010). A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J. 29, 3082–3093.Google Scholar

  • Bernstein, B.E., Ewan, B., Ian, D., Green, E.D., Chris, G., and Michael, S. (2012). An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57–74.Google Scholar

  • Bond, A.M., Vangompel, M.J., Sametsky, E.A., Clark, M.F., Savage, J.C., Disterhoft, J.F., and Kohtz, J.D. (2009). Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry. Nat. Neurosci. 12, 1020–1027.Google Scholar

  • Bouchard, M., Grote, D., Craven, S.E., Sun, Q., Steinlein, P., and Busslinger, M. (2005). Identification of Pax2-regulated genes by expression profiling of the mid-hindbrain organizer region. Development 132, 2633–2643.Google Scholar

  • Cahoy, J.D., Emery, B., Kaushal, A., Foo, L.C., Zamanian, J.L., Christopherson, K.S., Xing, Y., Lubischer, J.L., Krieg, P.A., Krupenko, S.A., et al. (2008). A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28, 264–278.Google Scholar

  • Chalei, V., Sansom, S.N., Kong, L., Lee, S., Montiel, J.F., Vance, K.W., and Ponting, C.P. (2014). The long non-coding RNA Dali is an epigenetic regulator of neural differentiation. eLife 3, e4530.Google Scholar

  • Chen, L.L. and Carmichael, G.G. (2010). Decoding the function of nuclear long non-coding RNAs. Curr. Opin. Cell Biol. 22, 357–364.Google Scholar

  • Clark, B.S. and Blackshaw, S. (2014). Long non-coding RNA-dependent transcriptional regulation in neuronal development and disease. Front. Genet. 5, 164.Google Scholar

  • Compagnucci, C., Di Siena, S., Bustamante, M.B., Di Giacomo, D., Di Tommaso, M., Maccarrone, M., Grimaldi, P., and Sette, C. (2013). Type-1 (CB1) cannabinoid receptor promotes neuronal differentiation and maturation of neural stem cells. PLoS One 8, e54271.Google Scholar

  • Derrien, T., Johnson, R., Bussotti, G., Tanzer, A., Djebali, S., Tilgner, H., Guernec, G., Martin, D., Merkel, A., Knowles, D.G., et al. (2012). The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 22, 1775–1789.Google Scholar

  • Fatica, A. and Bozzoni, I. (2014). Long non-coding RNAs: new players in cell differentiation and development. Nat. Rev. Genet. 15, 7–21.Google Scholar

  • Feng, J., Bi, C., Clark, B.S., Mady, R., Shah, P., and Kohtz, J.D. (2006). The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes Dev. 20, 1470–1484.Google Scholar

  • Grabowski, P. (2011). Alternative splicing takes shape during neuronal development. Curr. Opin. Genet. Dev. 21, 388–394.Google Scholar

  • Guillemot, F. (2007). Cell fate specification in the mammalian telencephalon. Prog. Neurobiol. 83, 37–52.Google Scholar

  • Guttman, M., Donaghey, J., Carey, B.W., Garber, M., Grenier, J.K., Munson, G., Young, G., Lucas, A.B., Ach, R., Bruhn, L., et al. (2011). lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477, 295–300.Google Scholar

  • Hu, W., Alvarez-Dominguez, J.R., and Lodish, H.F. (2012). Regulation of mammalian cell differentiation by long non-coding RNAs. EMBO Rep. 13, 971–983.Google Scholar

  • Huang, Y., Liu, N., Wang, J.P., Wang, Y.Q., Yu, X.L., Wang, Z.B., Cheng, X.C., and Zou, Q. (2012). Regulatory long non-coding RNA and its functions. J. Physiol. Biochem. 68, 611–618.Google Scholar

  • Huarte, M., Guttman, M., Feldser, D., Garber, M., Koziol, M.J., Kenzelmann-Broz, D., Khalil, A.M., Zuk, O., Amit, I., Rabani, M., et al. (2010). A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142, 409–419.Google Scholar

  • Ihrie, R.A. and Alvarez-Buylla, A. (2011). Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 70, 674–686.Google Scholar

  • Ishii, M., Han, J., Yen, H.Y., Sucov, H.M., Chai, Y., and Maxson, R.E. Jr. (2005). Combined deficiencies of Msx1 and Msx2 cause impaired patterning and survival of the cranial neural crest. Development. 132, 4937–4350.Google Scholar

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

  • Kohtz, J.D. (2014). Long non-coding RNAs learn the importance of being in vivo. Front. Genet. 5, 45.Google Scholar

  • Kohtz, J.D. and Fishell, G. (2004). Developmental regulation of EVF-1, a novel non-coding RNA transcribed upstream of the mouse Dlx6 gene. Gene Expr. Patterns 4, 407–412.Google Scholar

  • Law, A.J., Kleinman, J.E., Weinberger, D.R., and Weickert, C.S. (2007). Disease-associated intronic variants in the ErbB4 gene are related to altered ErbB4 splice-variant expression in the brain in schizophrenia. Hum. Molec. Genet. 16, 129–141.Google Scholar

  • Lee, J.T. (2012). Epigenetic regulation by long noncoding RNAs. Science 338, 1435–1439.Google Scholar

  • Lin, N., Chang, K.Y., Li, Z., Gates, K., Rana, Z.A., Dang, J., Zhang, D., Han, T., Yang, C.S., Cunningham, T.J., et al. (2014). An evolutionarily conserved long noncoding RNA TUNA controls pluripotency and neural lineage commitment. Mol. Cell 53, 1005–1019.Google Scholar

  • Lui, J.H., Hansen, D.V., and Kriegstein, A.R. (2011). Development and evolution of the human neocortex. Cell 146, 18–36.Google Scholar

  • Mattick, J.S. (2009). The genetic signatures of noncoding RNAs. PLoS Genet. 5, e1000459.Google Scholar

  • Mattick, J.S., Amaral, P.P., Dinger, M.E., Mercer, T.R., and Mehler, M.F. (2009). RNA regulation of epigenetic processes. Bioessays 31, 51–59.Google Scholar

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

  • Mercer, T.R. and Mattick, J.S. (2013). Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol. 20, 300–307.Google Scholar

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

  • Mercer, T.R., Dinger, M.E., and Mattick, J.S. (2009). Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 10, 155–159.Google Scholar

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

  • Ming, G.L. and Song, H. (2011). Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70, 687–702.Google Scholar

  • Mo, C.F., Wu, F.C., Tai, K.Y., Chang, W.C., Chang, K.W., Kuo, H.C., Ho, H.N., Chen, H.F., and Lin, S.P. (2015). Loss of non-coding RNA expression from the DLK1-DIO3 imprinted locus correlates with reduced neural differentiation potential in human embryonic stem cell lines. Stem Cell Res. Ther. 6, 1.Google Scholar

  • Moritz, E., Tony, G., Monika, H., Stefan, G., Maïwen, C.H., and Matthias, G., et al. (2012). Loss of the abundant nuclear non-coding rna malat1 is compatible with life and development. Rna Biology, 9, 1076–1087.Google Scholar

  • Morris, K.V., Santoso, S., Turner, A.M., Pastori, C., and Hawkins, P.G. (2008). Bidirectional transcription directs both transcriptional gene activation and suppression in human cells. PLoS Genet. 4, e1000258.Google Scholar

  • Nagano, T. and Fraser, P. (2011). No-nonsense functions for long noncoding RNAs. Cell 145, 178–181.Google Scholar

  • Nakata, K., Lipska, B.K., Hyde, T.M., Ye, T., Newburn, E.N., Morita, Y., Vakkalanka, R., Barenboim, M., Sei, Y., Weinberger, D.R., et al. (2009). DISC1 splice variants are upregulated in schizophrenia and associated with risk polymorphisms. Proc. Natl. Acad. Sci. USA 106, 15873–15878.Google Scholar

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

  • Ng, S.Y., Bogu, G.K., Soh, B.S., and Stanton, L.W. (2013). The long noncoding RNA RMST interacts with SOX2 to regulate neurogenesis. Mol. Cell 51, 349–359.Google Scholar

  • Onoguchi, M., Hirabayashi, Y., Koseki, H., and Gotoh, Y. (2012). A noncoding RNA regulates the neurogenin1 gene locus during mouse neocortical development. Proc. Natl. Acad. Sci. USA 109, 16939–16944.Google Scholar

  • Pandey, G.K., Mitra, S., Subhash, S., Hertwig, F., Kanduri, M., Mishra, K., Fransson, S., Ganeshram, A., Mondal, T., Bandaru, S., et al. (2014). The risk-associated long noncoding RNA NBAT-1 controls neuroblastoma progression by regulating cell proliferation and neuronal differentiation. Cancer Cell 26, 722–737.Google Scholar

  • Panganiban, G. and Rubenstein, J.L. (2002). Developmental functions of the Distal-less/Dlx homeobox genes. Development 129, 4371–4386.Google Scholar

  • Peschansky, V.J., Pastori, C., Zeier, Z., Motti, D., Wentzel, K., Velmeshev, D., Magistri, M., Bixby, J.L., Lemmon, V.P., Silva, J.P., et al. (2015). Changes in expression of the long non-coding RNA FMR4 associate with altered gene expression during differentiation of human neural precursor cells. Front. Genet. 6, 263.Google Scholar

  • Ponjavic, J., Oliver, P.L., Lunter, G., and Ponting, C.P. (2009). Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain. PLoS Genet. 5, e1000617.Google Scholar

  • Prasanth, K.V. and Spector, D.L. (2007). Eukaryotic regulatory RNAs: an answer to the ‘genome complexity’ conundrum. Genes Dev. 21, 11–42.Google Scholar

  • Ramos, A.D., Diaz, A., Nellore, A., Delgado, R.N., Park, K.Y., Gonzales-Roybal, G., Oldham, M.C., Song, J.S., and Lim, D.A. (2013). Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. Cell Stem Cell 12, 616–628.Google Scholar

  • Ramos, A.D., Andersen, R.E., Liu, S.J., Nowakowski, T.J., Hong, S.J., Gertz, C.C., Salinas, R.D., Zarabi, H., Kriegstein, A.R., and Lim, D.A. (2015). The long noncoding RNA Pnky regulates neuronal differentiation of embryonic and postnatal neural stem cells. Cell Stem Cell 16, 439–447.Google Scholar

  • Rapicavoli, N.A., Poth, E.M., and Blackshaw, S. (2010). The long noncoding RNA rncr2 directs mouse retinal cell specification. Bmc Dev. Biol. 10, 1–10.Google Scholar

  • Rapicavoli, N.A., Poth, E.M., Zhu, H., and Blackshaw, S. (2011). The long noncoding RNA six3os acts in trans to regulate retinal development by modulating six3 activity. Neural Dev. 6, 1–15.Google Scholar

  • Rinn, J.L. and Chang, H.Y. (2012). Genome regulation by long noncoding RNAs. Ann. Rev. Biochem. 81, 145–166.Google Scholar

  • Rinn, J.L., Kertesz, M., Wang, J.K., Squazzo, S.L., Xu, X., Brugmann, S.A., Goodnough, L.H., Helms, J.A., Farnham, P.J., Segal, E., et al. (2007). Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311–1323.Google Scholar

  • Sauvageau, M., Goff, L.A., Lodato, S., Bonev, B., Groff, A.F., Gerhardinger, C., Sanchez-Gomez, D.B., Hacisuleyman, E, Li, E., Spence, M., et al. (2013). Multiple knockout mouse models reveal lincRNAs are required for life and brain development. eLife 2, e01749.Google Scholar

  • Schwartz, J.C., Younger, S.T., Nguyen, N.B., Hardy, D.B., Monia, B.P., Corey, D.R., and Janowski, B.A. (2008). Antisense transcripts are targets for activating small RNAs. Nat. Struct. Mol. Biol. 15, 842–848.Google Scholar

  • Shinichi, N., Ip, J. Y., Go, S., Vidisha, T., Xinying, Z., & Tetsuro, H., et al. (2012). Malat1 is not an essential component of nuclear speckles in mice. Rna-a Publication of the Rna Society, 18, 1487–99.Google Scholar

  • Sone, M., Hayashi, T., Tarui, H., Agata, K., Takeichi, M., and Nakagawa, S. (2007). The mRNA-like noncoding RNA Gomafu constitutes a novel nuclear domain in a subset of neurons. J. Cell Sci. 120, 2498–2506.Google Scholar

  • Stefan, W., Manolis, K., and Manuel, G. (2014). Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals. Genome Res. 24, 616–628.Google Scholar

  • Tochitani, S. and Hayashizaki, Y. (2008). Nkx2.2 antisense RNA overexpression enhanced oligodendrocytic differentiation. Biochem. Biophys. Res. Commun. 372, 691–696.Google Scholar

  • Tripathi, V., Ellis, J.D., Shen, Z., Song, D.Y., Pan, Q., Watt, A.T., Freier, S.M., Bennett, C.F., Sharma, A., Bubulya, P.A., et al. (2010). The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol. Cell 39, 925–938.Google Scholar

  • Tsai, M.C., Manor, O., Wan, Y., Mosammaparast, N., Wang, J.K., Lan, F., Shi, Y., Segal, E., and Chang, H.Y. (2010). Long noncoding RNA as modular scaffold of histone modification complexes. Science 329, 689–693.Google Scholar

  • Tsuiji, H., Yoshimoto, R., Hasegawa, Y., Furuno, M., Yoshida, M., and Nakagawa, S. (2011). Competition between a noncoding exon and introns: Gomafu contains tandem UACUAAC repeats and associates with splicing factor-1. Genes Cells 16, 479–490.Google Scholar

  • Uhde, C.W., Vives, J., Jaeger, I., and Li, M. (2010). Rmst is a novel marker for the mouse ventral mesencephalic floor plate and the anterior dorsal midline cells. PLoS One 5, e8641.Google Scholar

  • Washietl, S., Kellis, M., Garber, M. (2014). Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals. Genome Res. 24, 616–628.Google Scholar

  • Wu, P., Zuo, X., Deng, H., Liu, X., Liu, L., and Ji, A. (2013). Roles of long noncoding RNAs in brain development, functional diversification and neurodegenerative diseases. Brain Res. Bull. 97, 69–80.Google Scholar

  • Yanling, W., Dye, C.A., Vikaas, S., Long, J.E., Estrada, R.C., and Tomas, R., et al. (2010). Dlx5 and dlx6 regulate the development of parvalbumin-expressing cortical interneurons. Journal of Neuroscience the Official Journal of the Society for Neuroscience, 30, 5334–5345.Google Scholar

  • Yu, W., Gius, D., Onyango, P., Muldoon-Jacobs, K., Karp, J., Feinberg, A.P., and Cui, H. (2008). Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature 451, 202–206.Google Scholar

  • Zhang, B., Arun, G. Mao, Y.S., Lazar, Z., Hung, G., Bhattacharjee, G., Xiao, X., Booth, C.J., Wu, J., Zhang, C. et al. (2012). The lncRNA malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep. 2, 111–123.Google Scholar

About the article

Corresponding authors: Ming Lu, Department of Neurosurgery, the Second Affiliated Hospital of Hunan Normal University (PLA 163 Hospital), Cangsha 41000, China, e-mail: ; and Ying Xia, Department of Neurosurgery, Affiliated Haikou Hospital, Xiangya School of Central South University, Haikou 570100, China, e-mail:

aLei Wang and Yan Liu: These authors contributed equally to this work.


Received: 2015-10-29

Accepted: 2016-02-06

Published Online: 2016-03-04

Published in Print: 2016-07-01


Conflict of interest disclosure: The authors have no conflicts of interest to disclose.


Citation Information: Reviews in the Neurosciences, ISSN (Online) 2191-0200, ISSN (Print) 0334-1763, DOI: https://doi.org/10.1515/revneuro-2015-0061.

Export Citation

©2016 by De Gruyter. Copyright Clearance Center

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Lei Wang, Zhengtao Yu, Shaiqi Sun, Jun Peng, Rongjun Xiao, Shengpan Chen, Xiaokun Zuo, Quan Cheng, and Ying Xia
Reviews in the Neurosciences, 2017, Volume 28, Number 4
[2]
Lei Wang, Yujia Deng, Da Duan, Shuaiqi Sun, Lite Ge, Yi Zhuo, Ting Yuan, Pei Wu, Hao Wang, Ming Lu, Ying Xia, and Austin John Cooney
PLOS ONE, 2017, Volume 12, Number 2, Page e0171359

Comments (0)

Please log in or register to comment.
Log in