Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter June 5, 2014

MicroRNAs in central nervous system development

  • Néstor F. Díaz , Mónica S. Cruz-Reséndiz , Héctor Flores-Herrera , Guadalupe García-López and Anayansi Molina-Hernández EMAIL logo

Abstract

During early and late embryo neurodevelopment, a large number of molecules work together in a spatial and temporal manner to ensure the adequate formation of an organism. Diverse signals participate in embryo patterning and organization synchronized by time and space. Among the molecules that are expressed in a temporal and spatial manner, and that are considered essential in several developmental processes, are the microRNAs (miRNAs). In this review, we highlight some important aspects of the biogenesis and function of miRNAs as well as their participation in ectoderm commitment and their role in central nervous system (CNS) development. Instead of giving an extensive list of miRNAs involved in these processes, we only mention those miRNAs that are the most studied during the development of the CNS as well as the most likely mRNA targets for each miRNA and its protein functions.


Corresponding author: Anayansi Molina-Hernández, Departamento de Biología Celular, Instituto Nacional de Perinatología, Montes Urales 800, Colonia Lomas de Virreyes, Miguel Hidalgo, CP 11000, México, e-mail: ;

Acknowledgments

The research of our group is supported by the Instituto Nacional de Perinatología and the Consejo Nacional de Ciencia y Tecnología. M.S. Cruz-Reséndiz received a Consejo Nacional de Ciencia y Tecnología fellowship at the Programa de Posgrado en Ciencias Biológicas at the Universidad Nacional Autónoma de México. We thank David Connolly and Adam Pixler for the language editing and correction.

Conflict of interest statement

Competing interests: The authors have declared that no competing interests exist.

Authors’ contributions: All authors participated in the preparation of the manuscript and read and approved the final manuscript.

References

Aboobaker, A.A., Tomancak, P., Patel, N., Rubin, G.M., and Lai, E.C. (2005). Drosophila microRNAs exhibit diverse spatial expression patterns during embryonic development. Proc. Natl. Acad. Sci. USA 102, 18017–18022.10.1073/pnas.0508823102Search in Google Scholar

Alvarez-Buylla, A., Kohwi, M., Nguyen, T.M., and Merkle, F.T. (2008). The heterogeneity of adult neural stem cells and the emerging complexity of their niche. Cold Spring Harb. Symp. Quant. Biol. 73, 357–365.10.1101/sqb.2008.73.019Search in Google Scholar

Barbato, C., Ruberti, F., Pieri, M., Vilardo, E., Costanzo, M., Ciotti, M.T., Zona, C., and Cogoni, C. (2010). MicroRNA-92 modulates K+ Cl- co-transporter KCC2 expression in cerebellar granule neurons. J. Neurochem. 113, 591–600.10.1111/j.1471-4159.2009.06560.xSearch in Google Scholar

Barca-Mayo, O. and De Pietri Tonelli, D. (2014). Convergent microRNA actions coordinate neocortical development. Cell. MoLi, L.fe Sci. DOI 10.1007/s00018-014-1576-5.Search in Google Scholar

Bartel, D.P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.10.1016/S0092-8674(04)00045-5Search in Google Scholar

Bartel, D.P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233.10.1016/j.cell.2009.01.002Search in Google Scholar PubMed PubMed Central

Berezikov, E., Chung, W.J., Willis, J., Cuppen, E., and Lai, E.C. (2007). Mammalian mirtron genes. Mol. Cell. 28, 328–336.10.1016/j.molcel.2007.09.028Search in Google Scholar PubMed PubMed Central

Bhattacharyya, S.N., Habermacher, R., Martine, U., Closs, E.I., and Filipowicz, W. (2006). Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111–1124.10.1016/j.cell.2006.04.031Search in Google Scholar PubMed

Blaesse, P., Airaksinen, M.S., Rivera, C., and Kaila, K. (2009). Cation-chloride cotransporters and neuronal function. Neuron 61, 820–838.10.1016/j.neuron.2009.03.003Search in Google Scholar PubMed

Boeri, M., Verri, C., Conte, D., Roz, L., Modena, P., Facchinetti, F., Calabro, E., Croce, C.M., Pastorino, U., and Sozzi, G. (2011). MicroRNA signatures in tissues and plasma predict development and prognosis of computed tomography detected lung cancer. Proc. Natl. Acad. Sci. USA 108, 3713–3718.10.1073/pnas.1100048108Search in Google Scholar PubMed PubMed Central

Borchert, G.M., Lanier, W., and Davidson, B.L. (2006). RNA polymerase III transcribes human microRNAs. Nat. Struct. Mol. Biol. 13, 1097–1101.10.1038/nsmb1167Search in Google Scholar PubMed

Candiani, S., Moronti, L., De Pietri Tonelli, D., Garbarino, G., and Pestarino, M. (2011). A study of neural-related microRNAs in the developing amphioxus. Evodevo 2, 15.10.1186/2041-9139-2-15Search in Google Scholar

Cao, X., Pfaff, S.L., and Gage, F.H. (2007). A functional study of miR-124 in the developing neural tube. Genes Dev. 21, 531–536.10.1101/gad.1519207Search in Google Scholar

Caygill, E.E. and Johnston, L.A. (2008). Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs. Curr. Biol. 18, 943–950.10.1016/j.cub.2008.06.020Search in Google Scholar

Cifuentes, D., Xue, H., Taylor, D.W., Patnode, H., Mishima, Y., Cheloufi, S., Ma, E., Mane, S., Hannon, G.J., Lawson, N.D., et al. (2010). A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 328, 1694–1698.10.1126/science.1190809Search in Google Scholar

Cimmino, A., Calin, G.A., Fabbri, M., Iorio, M.V., Ferracin, M., Shimizu, M., Wojcik, S.E., Aqeilan, R.I., Zupo, S., Dono, M., et al. (2005). miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc. Natl. Acad. Sci. USA 102, 13944–13949.10.1073/pnas.0506654102Search in Google Scholar

Colas, A.R., McKeithan, W.L., Cunningham, T.J., Bushway, P.J., Garmire, L.X., Duester, G., Subramaniam, S., and Mercola, M. (2012). Whole-genome microRNA screening identifies let-7 and mir-18 as regulators of germ layer formation during early embryogenesis. Genes Dev. 26, 2567–2579.10.1101/gad.200758.112Search in Google Scholar

Conaco, C., Otto, S., Han, J.J., and Mandel, G. (2006). Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl. Acad. Sci. USA 103, 2422–2427.10.1073/pnas.0511041103Search in Google Scholar

Cortez, M.A. and Calin, G.A. (2009). MicroRNA identification in plasma and serum: a new tool to diagnose and monitor diseases. Expert Opin. Biol. Ther. 9, 703–711.10.1517/14712590902932889Search in Google Scholar

Cortez, M.A., Bueso-Ramos, C., Ferdin, J., Lopez-Berestein, G., Sood, A.K., and Calin, G.A. (2011). MicroRNAs in body fluids – the mix of hormones and biomarkers. Nat. Rev. Clin. Oncol. 8, 467–477.10.1038/nrclinonc.2011.76Search in Google Scholar

Chalfie, M., Horvitz, H.R., and Sulston, J.E. (1981). Mutations that lead to reiterations in the cell lineages of C. elegans. Cell 24, 59–69.10.1016/0092-8674(81)90501-8Search in Google Scholar

Cheloufi, S., Dos Santos, C.O., Chong, M.M., and Hannon, G.J. (2010). A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 465, 584–589.10.1038/nature09092Search in Google Scholar PubMed PubMed Central

Chen, X., Ba, Y., Ma, L., Cai, X., Yin, Y., Wang, K., Guo, J., Zhang, Y., Chen, J., Guo, X., et al. (2008). Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 18, 997–1006.10.1038/cr.2008.282Search in Google Scholar PubMed

Chendrimada, T.P., Gregory, R.I., Kumaraswamy, E., Norman. J., Cooch, N., Nishikura, K., and Shiekhattar, R. (2005). TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740–744.10.1038/nature03868Search in Google Scholar PubMed PubMed Central

Cheng, L.C., Pastrana, E., Tavazoie, M., and Doetsch, F. (2009). miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 12, 399–408.10.1038/nn.2294Search in Google Scholar PubMed PubMed Central

Choi, P.S., Zakhary, L., Choi, Y.W., Caron, S., Alvarez-Saavedra, E., Miska, E.A., McManus, M., Harfe, B., Giraldez, A.J., Horvitz, H.R., et al. (2008). Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron 57, 41–55.10.1016/j.neuron.2007.11.018Search in Google Scholar PubMed PubMed Central

Chung, W.J., Agius, P., Westholm, J.O., Chen, M., Okamura, K., Robine, N., Leslie, C.S., and Lai, E.C. (2011). Computational and experimental identification of mirtrons in Drosophila melanogaster and Caenorhabditis elegans. Genome Res. 21, 286–300.10.1101/gr.113050.110Search in Google Scholar PubMed PubMed Central

Darnell, D.K., Kaur, S., Stanislaw, S., Konieczka, J.H., Yatskievych, T.A., and Antin, P.B. (2006). MicroRNA expression during chick embryo development. Dev. Dyn. 235, 3156–3165.10.1002/dvdy.20956Search in Google Scholar PubMed

Davis, T.H., Cuellar, T.L., Koch, S.M., Barker, A.J., Harfe, B.D., McManus, M.T., and Ullian, E.M. (2008). Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J. Neurosci. 28, 4322–4330.10.1523/JNEUROSCI.4815-07.2008Search in Google Scholar PubMed PubMed Central

Delaloy, C., Liu, L., Lee, J.A., Su, H., Shen, F., Yang, Y.G., Young, W.L., Ivey, K.N., and Gao, F.B. (2010). MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell. 6, 323–335.10.1016/j.stem.2010.02.015Search in Google Scholar PubMed PubMed Central

Doench, J.G. and Sharp, P.A. (2004). Specificity of microRNA target selection in translational repression. Genes Dev. 18, 504–511.10.1101/gad.1184404Search in Google Scholar PubMed PubMed Central

Du, T. and Zamore, P.D. (2005). microPrimer: the biogenesis and function of microRNA. Development 132, 4645–4652.10.1242/dev.02070Search in Google Scholar

Du, Z.W., Ma, L.X., Phillips, C., and Zhang, S.C. (2013). miR-200 and miR-96 families repress neural induction from human embryonic stem cells. Development 140, 2611–2618.10.1242/dev.092809Search in Google Scholar

Fiore, R., Siegel, G., and Schratt, G. (2008). MicroRNA function in neuronal development, plasticity and disease. Biochim. Biophys. Acta 1779, 471–478.10.1016/j.bbagrm.2007.12.006Search in Google Scholar

Frank, F., Sonenberg, N., and Nagar, B. (2010). Structural basis for 5′-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 465, 818–822.10.1038/nature09039Search in Google Scholar

Friedman, R.C., Farh, K.K., Burge, C.B., and Bartel, D.P. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92–105.10.1101/gr.082701.108Search in Google Scholar

Gage, F.H., Kempermann, G., Palmer, T.D., Peterson, D.A., and Ray, J. (1998). Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol. 36, 249–266.10.1002/(SICI)1097-4695(199808)36:2<249::AID-NEU11>3.0.CO;2-9Search in Google Scholar

Gao, F.B. (2010). Context-dependent functions of specific microRNAs in neuronal development. Neural Dev. 5, 25.10.1186/1749-8104-5-25Search in Google Scholar

Ghildiyal, M., Xu, J., Seitz, H., Weng, Z., and Zamore, P.D. (2010). Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. RNA 16, 43–56.10.1261/rna.1972910Search in Google Scholar

Gil-Perotin, S., Alvarez-Buylla, A., and Garcia-Verdugo, J.M. (2009). Identification and characterization of neural progenitor cells in the adult mammalian brain. Adv. Anat. Embryol. Cell. Biol. 203, 1–101, ix.Search in Google Scholar

Gilad, S., Meiri, E., Yogev, Y., Benjamin, S., Lebanony, D., Yerushalmi, N., Benjamin, H., Kushnir, M., Cholakh, H., Melamed, N., et al. (2008). Serum microRNAs are promising novel biomarkers. PLoS One 3, e3148.10.1371/journal.pone.0003148Search in Google Scholar

Greene, N.D. and Copp, A.J. (2012). Could microRNAs be biomarkers for neural tube defects? J. Neurochem. 122, 485–486.10.1111/j.1471-4159.2012.07800.xSearch in Google Scholar

Griffiths-Jones, S., Grocock, R.J., Van Dongen, S., Bateman, A., and Enright, A.J. (2006). miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34, D140–D144.10.1093/nar/gkj112Search in Google Scholar PubMed PubMed Central

Gu, H., Li, H., Zhang, L., Luan, H., Huang, T., Wang, L., Fan, Y., Zhang, Y., Liu, X., Wang, W., et al. (2012). Diagnostic role of microRNA expression profile in the serum of pregnant women with fetuses with neural tube defects. J. Neurochem. 122, 641–649.10.1111/j.1471-4159.2012.07812.xSearch in Google Scholar PubMed

Han, J., Lee, Y., Yeom, K.H., Nam, J.W., Heo, I., Rhee, J.K., Sohn, S.Y., Cho, Y., Zhang, B.T., and Kim, V.N. (2006). Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125, 887–901.10.1016/j.cell.2006.03.043Search in Google Scholar PubMed

Hebert, S.S. and De Strooper, B. (2007). Molecular biology. miRNAs in neurodegeneration. Science 317, 1179–1180.10.1126/science.1148530Search in Google Scholar PubMed

Hutchison, M., Berman, K.S., and Cobb, M.H. (1998). Isolation of TAO1, a protein kinase that activates MEKs in stress-activated protein kinase cascades. J. Biol. Chem. 273, 28625–28632.10.1074/jbc.273.44.28625Search in Google Scholar PubMed

Hutvagner, G., McLachlan, J., Pasquinelli, A.E., Balint, E., Tuschl, T., and Zamore, P.D. (2001). A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293, 834–838.10.1126/science.1062961Search in Google Scholar PubMed

Ji, F., Lv, X., and Jiao, J. (2013). The role of microRNAs in neural stem cells and neurogenesis. J. Genet. Genomics 40, 61–66.10.1016/j.jgg.2012.12.008Search in Google Scholar PubMed

Kapsimali, M., Kloosterman, W.P., De Bruijn, E., Rosa, F., Plasterk, R.H., and Wilson, S.W. (2007). MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biol. 8, R173.10.1186/gb-2007-8-8-r173Search in Google Scholar PubMed PubMed Central

Kaspi, H., Chapnik, E., Levy, M., Beck, G., Hornstein, E., and Soen, Y. (2013). Brief report: miR-290-295 regulate embryonic stem cell differentiation propensities by repressing Pax6. Stem Cells 31, 2266–2272.10.1002/stem.1465Search in Google Scholar PubMed

Kim, J., Inoue, K., Ishii, J., Vanti, W.B., Voronov, S.V., Murchison, E., Hannon, G., and Abeliovich, A. (2007). A microRNA feedback circuit in midbrain dopamine neurons. Science 317, 1220–1224.10.1126/science.1140481Search in Google Scholar PubMed PubMed Central

Kloosterman, W.P., Wienholds, E., De Bruijn, E., Kauppinen, S., and Plasterk, R.H. (2006). In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nat. Methods 3, 27–29.10.1038/nmeth843Search in Google Scholar

Kozomara, A. and Griffiths-Jones, S. (2011). miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39, D152–D157.10.1093/nar/gkq1027Search in Google Scholar

Krichevsky, A.M., King, K.S., Donahue, C.P., Khrapko, K., and Kosik, K.S. (2003). A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 9, 1274–1281.10.1261/rna.5980303Search in Google Scholar

Krichevsky, A.M., Sonntag, K.C., Isacson, O., and Kosik, K.S. (2006). Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24, 857–864.10.1634/stemcells.2005-0441Search in Google Scholar

Kulkarni, M., Ozgur, S., and Stoecklin, G. (2010). On track with P-bodies. Biochem. Soc. Trans. 38, 242–251.10.1042/BST0380242Search in Google Scholar

Lagos-Quintana, M., Rauhut, R., Meyer, J., Borkhardt, A., and Tuschl, T. (2003). New microRNAs from mouse and human. RNA 9, 175–179.10.1261/rna.2146903Search in Google Scholar

Le, M.T., Xie, H., Zhou, B., Chia, P.H., Rizk, P., Um, M., Udolph, G., Yang, H., Lim, B., and Lodish, H.F. (2009). MicroRNA-125b promotes neuronal differentiation in human cells by repressing multiple targets. Mol. Cell. Biol. 29, 5290–5305.10.1128/MCB.01694-08Search in Google Scholar

Le, M.T.N., Teh, C., Shyh-Chang, N., Korzh, V., Lodish, H.F., and Lim, B. (2010). Function of miR-125b in zebrafish neurogenesis. Int. J. Biol. Life Sci. Eng. 4, 635–640.Search in Google Scholar

Le, M.T., Shyh-Chang, N., Khaw, S.L., Chin, L., Teh, C., Tay, J., O’Day, E., Korzh, V., Yang, H., Lal, A., et al. (2011). Conserved regulation of p53 network dosage by microRNA-125b occurs through evolving miRNA-target gene pairs. PLoS Genet. 7, e1002242.10.1371/journal.pgen.1002242Search in Google Scholar

Lee, R.C. and Ambros, V. (2001). An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862–864.10.1126/science.1065329Search in Google Scholar

Lee, R.C., Feinbaum, R.L., and Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854.10.1016/0092-8674(93)90529-YSearch in Google Scholar

Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S., et al. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415–419.10.1038/nature01957Search in Google Scholar

Lewis, B. P., Shih, I.H., Jones-Rhoades, M.W., Bartel, D.P., and Burge, C.B. (2003). Prediction of mammalian microRNA targets. Cell 115, 787–798.10.1016/S0092-8674(03)01018-3Search in Google Scholar

Lichner, Z., Pall, E., Kerekes, A., Pallinger, E., Maraghechi, P., Bosze, Z., and Gocza, E. (2011). The miR-290-295 cluster promotes pluripotency maintenance by regulating cell cycle phase distribution in mouse embryonic stem cells. Differentiation 81, 11–24.10.1016/j.diff.2010.08.002Search in Google Scholar PubMed

Lim, L.P., Lau, N.C., Garrett-Engele, P., Grimson, A., Schelter, J.M., Castle, J., Bartel, D.P., Linsley, S.P., and Johnson, J.M. (2005). Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769–773.10.1038/nature03315Search in Google Scholar PubMed

Liu, N., Okamura, K., Tyler, D.M., Phillips, M.D., Chung, W.J., and Lai, E.C. (2008). The evolution and functional diversification of animal microRNA genes. Cell Res. 18, 985–996.10.1038/cr.2008.278Search in Google Scholar PubMed PubMed Central

Llave, C., Xie, Z., Kasschau, K.D., and Carrington, J.C. (2002). Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053–2056.10.1126/science.1076311Search in Google Scholar PubMed

Maiorano, N.A. and Mallamaci, A. (2009). Promotion of embryonic cortico-cerebral neuronogenesis by miR-124. Neural Dev. 4, 40.10.1186/1749-8104-4-40Search in Google Scholar PubMed PubMed Central

Makeyev, E.V., Zhang, J., Carrasco, M.A., and Maniatis, T. (2007). The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell. 27, 435–448.10.1016/j.molcel.2007.07.015Search in Google Scholar PubMed PubMed Central

Marcelis, C.L., Hol, F.A., Graham, G.E., Rieu, P.N., Kellermayer, R., Meijer, R.P., Lugtenberg, D., Scheffer, H., Van Bokhoven, H., Brunner, H.G., et al. (2008). Genotype-phenotype correlations in MYCN-related Feingold syndrome. Hum. Mutat. 29, 1125–1132.10.1002/humu.20750Search in Google Scholar PubMed

Marson, A., Levine, S.S., Cole, M.F., Frampton, G.M., Brambrink, T., Johnstone, S., Guenther, M.G., Johnston, W.K., Wernig, M., Newman, J., et al. (2008). Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134, 521–533.10.1016/j.cell.2008.07.020Search in Google Scholar PubMed PubMed Central

Miska, E.A., Alvarez-Saavedra, E., Townsend, M., Yoshii, A., Sestan, N., Rakic, P., Constantine-Paton, M., and Horvitz, H.R. (2004). Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol. 5, R68.10.1186/gb-2004-5-9-r68Search in Google Scholar PubMed PubMed Central

Miska, E.A., Alvarez-Saavedra, E., Abbott, A.L., Lau, N.C., Hellman, A.B., McGonagle, S.M., Bartel, D.P., Ambros, V.R., and Horvitz, H.R. (2007). Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet. 3, e215.10.1371/journal.pgen.0030215Search in Google Scholar PubMed PubMed Central

Mogilyansky, E. and Rigoutsos, I. (2013). The miR-17/92 cluster: a comprehensive update on its genomics, genetics, functions and increasingly important and numerous roles in health and disease. Cell Death Differ. 20, 1603–1614.10.1038/cdd.2013.125Search in Google Scholar PubMed PubMed Central

Nan, Y., Han, L., Zhang, A., Wang, G., Jia, Z., Yang, Y., Yue, X., Pu, P., Zhong, Y., and Kang, C. (2010). miRNA-451 plays a role as tumor suppressor in human glioma cells. Brain Res. 1359, 14–21.10.1016/j.brainres.2010.08.074Search in Google Scholar PubMed

Nielsen, J.A., Lau, P., Maric, D., Barker, J.L., and Hudson, L.D. (2009). Integrating microRNA and mRNA expression profiles of neuronal progenitors to identify regulatory networks underlying the onset of cortical neurogenesis. BMC Neurosci. 10, 98.10.1186/1471-2202-10-98Search in Google Scholar PubMed PubMed Central

Olguin, P., Oteiza, P., Gamboa, E., Gomez-Skarmeta, J.L., and Kukuljan, M. (2006). RE-1 silencer of transcription/neural restrictive silencer factor modulates ectodermal patterning during Xenopus development. J. Neurosci. 26, 2820–2829.10.1523/JNEUROSCI.5037-05.2006Search in Google Scholar PubMed PubMed Central

Olsen, P.H. and Ambros, V. (1999). The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671–680.10.1006/dbio.1999.9523Search in Google Scholar PubMed

Papagiannakopoulos, T. and Kosik, K.S. (2009). MicroRNA-124: micromanager of neurogenesis. Cell Stem Cell 4, 375–376.10.1016/j.stem.2009.04.007Search in Google Scholar PubMed

Qureshi, I.A. and Mehler, M.F. (2012). Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nat. Rev. Neurosci. 13, 528–541.10.1038/nrn3234Search in Google Scholar PubMed PubMed Central

Rabinowits, G., Gercel-Taylor, C., Day, J.M., Taylor, D.D., and Kloecker, G.H. (2009). Exosomal microRNA: a diagnostic marker for lung cancer. Clin. Lung Cancer 10, 42–46.10.3816/CLC.2009.n.006Search in Google Scholar PubMed

Rajasekharan, S. and Kennedy, T.E. (2009). The netrin protein family. Genome Biol. 10, 239.10.1186/gb-2009-10-9-239Search in Google Scholar

Raman, M., Earnest, S., Zhang, K., Zhao, Y., and Cobb, M.H. (2007). TAO kinases mediate activation of p38 in response to DNA damage. EMBO J. 26, 2005–2014.10.1038/sj.emboj.7601668Search in Google Scholar

Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R., and Ruvkun, G. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901–906.10.1038/35002607Search in Google Scholar

Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., and Bartel, D.P. (2002). Prediction of plant microRNA targets. Cell 110, 513–520.10.1016/S0092-8674(02)00863-2Search in Google Scholar

Roese-Koerner, B., Stappert, L., Koch, P., Brustle, O., and Borghese, L. (2013). Pluripotent stem cell-derived somatic stem cells as tool to study the role of microRNAs in early human neural development. Curr. Mol. Med. 13, 707–722.10.2174/1566524011313050003Search in Google Scholar PubMed

Ruby, J.G., Jan, C.H., and Bartel, D.P. (2007). Intronic microRNA precursors that bypass Drosha processing. Nature 448, 83–86.10.1038/nature05983Search in Google Scholar PubMed PubMed Central

Sarver, A.L., Li, L., and Subramanian, S. (2010). MicroRNA miR-183 functions as an oncogene by targeting the transcription factor EGR1 and promoting tumor cell migration. Cancer Res. 70, 9570–9580.10.1158/0008-5472.CAN-10-2074Search in Google Scholar PubMed

Saurat, N., Andersson, T., Vasistha, N.A., Molnar, Z., and Livesey, F.J. (2013). Dicer is required for neural stem cell multipotency and lineage progression during cerebral cortex development. Neural Dev. 8, 14.10.1186/1749-8104-8-14Search in Google Scholar PubMed PubMed Central

Schaefer, A., O’Carroll, D., Tan, C.L., Hillman, D., Sugimori, M., Llinas, R., and Greengard, P. (2007). Cerebellar neurodegeneration in the absence of microRNAs. J. Exp. Med. 204, 1553–1558.10.1084/jem.20070823Search in Google Scholar PubMed PubMed Central

Sempere, L.F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., and Ambros, V. (2004). Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 5, R13.10.1186/gb-2004-5-3-r13Search in Google Scholar PubMed PubMed Central

Seo, S., Lim, J.W., Yellajoshyula, D., Chang, L.W., and Kroll, K.L. (2007). Neurogenin and NeuroD direct transcriptional targets and their regulatory enhancers. EMBO J. 26, 5093–5108.10.1038/sj.emboj.7601923Search in Google Scholar PubMed PubMed Central

Smirnova, L., Grafe, A., Seiler, A., Schumacher, S., Nitsch, R., and Wulczyn, F.G. (2005). Regulation of miRNA expression during neural cell specification. Eur. J. Neurosci. 21, 1469–1477.10.1111/j.1460-9568.2005.03978.xSearch in Google Scholar PubMed

Suter, D.M., Tirefort, D., Julien, S., and Krause, K.H. (2009). A Sox1 to Pax6 switch drives neuroectoderm to radial glia progression during differentiation of mouse embryonic stem cells. Stem Cells 27, 49–58.10.1634/stemcells.2008-0319Search in Google Scholar PubMed

Takayama, C. and Inoue, Y. (2007). Developmental localization of potassium chloride co-transporter 2 (KCC2) in the Purkinje cells of embryonic mouse cerebellum. Neurosci. Res. 57, 322–325.10.1016/j.neures.2006.10.016Search in Google Scholar PubMed

Taylor, D.D. and Gercel-Taylor, C. (2008). MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110, 13–21.10.1016/j.ygyno.2008.04.033Search in Google Scholar PubMed

Valencia-Sanchez, M.A., Liu, J., Hannon, G.J., and Parker, R. (2006). Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 20, 515–524.10.1101/gad.1399806Search in Google Scholar PubMed

Visvanathan, J., Lee, S., Lee, B., Lee, J.W., and Lee, S.K. (2007). The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 21, 744–749.10.1101/gad.1519107Search in Google Scholar PubMed PubMed Central

Weston, M.D., Pierce, M.L., Rocha-Sanchez, S., Beisel, K.W., and Soukup, G.A. (2006). MicroRNA gene expression in the mouse inner ear. Brain Res. 1111, 95–104.10.1016/j.brainres.2006.07.006Search in Google Scholar PubMed

Wienholds, E. and Plasterk, R.H. (2005). MicroRNA function in animal development. FEBS Lett. 579, 5911–5922.10.1016/j.febslet.2005.07.070Search in Google Scholar PubMed

Wienholds, E., Kloosterman, W.P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., De Bruijn, E., Horvitz, H.R., Kauppinen, S., and Plasterk, R.H. (2005). MicroRNA expression in zebrafish embryonic development. Science 309, 310–311.10.1126/science.1114519Search in Google Scholar PubMed

Wightman, B., Ha, I., and Ruvkun, G. (1993). Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855–862.10.1016/0092-8674(93)90530-4Search in Google Scholar

Wu, L. and Belasco, J.G. (2005). Micro-RNA regulation of the mammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells. Mol. Cell. Biol. 25, 9198–9208.10.1128/MCB.25.21.9198-9208.2005Search in Google Scholar

Wu, M.F. and Wang, S.G. (2008). Human TAO kinase 1 induces apoptosis in SH-SY5Y cells. Cell. Biol. Int. 32, 151–156.10.1016/j.cellbi.2007.08.006Search in Google Scholar

Yang, J.S. and Lai, E.C. (2011). Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol. Cell. 43, 892–903.10.1016/j.molcel.2011.07.024Search in Google Scholar

Yang, J.S., Maurin, T., Robine, N., Rasmussen, K.D., Jeffrey, K.L., Chandwani, R., Papapetrou, E.P., Sadelain, M., O’Carroll, D., and Lai, E.C. (2010). Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc. Natl. Acad. Sci. USA 107, 15163–15168.10.1073/pnas.1006432107Search in Google Scholar

Yekta, S., Shih, I.H., and Bartel, D.P. (2004). MicroRNA-directed cleavage of HOXB8 mRNA. Science 304, 594–596.10.1126/science.1097434Search in Google Scholar

Yoo, A.S., Staahl, B.T., Chen, L., and Crabtree, G.R. (2009). MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460, 642–646.10.1038/nature08139Search in Google Scholar

Yu, J.Y., Chung, K.H., Deo, M., Thompson, R.C., and Turner, D.L. (2008). MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Exp. Cell. Res. 314, 2618–2633.10.1016/j.yexcr.2008.06.002Search in Google Scholar

Yu, B., Ma, H., Du, Z., Hong, Y., Sang, M., Liu, Y., and Shi, Y. (2011). Involvement of calmodulin and actin in directed differentiation of rat cortical neural stem cells into neurons. Int. J. Mol. Med. 28, 739–744.Search in Google Scholar

Zeng, Y., Wagner, E.J., and Cullen, B.R. (2002). Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. Mol. Cell. 9, 1327–1333.10.1016/S1097-2765(02)00541-5Search in Google Scholar

Zhang, X., Huang, C.T., Chen, J., Pankratz, M.T., Xi, J., Li, J., Yang, Y., Lavaute, T.M., Li, X.J., Ayala, M., et al. (2010). Pax6 is a human neuroectoderm cell fate determinant. Cell Stem Cell 7, 90–100.10.1016/j.stem.2010.04.017Search in Google Scholar PubMed PubMed Central

Zhang, Z., Li, S., and Cheng, S.Y. (2013). The miR-183 approximately 96 approximately 182 cluster promotes tumorigenesis in a mouse model of medulloblastoma. J. Biomed. Res. 27, 486–494.10.7555/JBR.27.20130010Search in Google Scholar

Zhao, C., Sun, G., Li, S., and Shi, Y. (2009). A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat. Struct. Mol. Biol. 16, 365–371.10.1038/nsmb.1576Search in Google Scholar PubMed PubMed Central

Received: 2014-2-17
Accepted: 2014-5-13
Published Online: 2014-6-5
Published in Print: 2014-10-1

©2014 by De Gruyter

Downloaded on 23.2.2024 from https://www.degruyter.com/document/doi/10.1515/revneuro-2014-0014/html
Scroll to top button