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.
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.0508823102Suche 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.2008.73.019Suche 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.xSuche 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.Suche in Google Scholar
Bartel, D.P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.10.1016/S0092-8674(04)00045-5Suche in Google Scholar
Bartel, D.P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233.10.1016/j.cell.2009.01.002Suche 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.2007.09.028Suche 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.2006.04.031Suche 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.2009.03.003Suche 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.1100048108Suche 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/nsmb1167Suche 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, 15.10.1186/2041-9139-2-15Suche 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.1519207Suche 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.2008.06.020Suche 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.1190809Suche 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.0506654102Suche 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.200758.112Suche 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.0511041103Suche 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, 703–711.10.1517/14712590902932889Suche 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.2011.76Suche 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)90501-8Suche 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/nature09092Suche 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.2008.282Suche 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/nature03868Suche 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.2294Suche 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.2007.11.018Suche 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.113050.110Suche 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.20956Suche 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.4815-07.2008Suche 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.2010.02.015Suche 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.1184404Suche 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.02070Suche 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.092809Suche 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.2007.12.006Suche 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/nature09039Suche 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.082701.108Suche 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;2-9Suche in Google Scholar
Gao, F.B. (2010). Context-dependent functions of specific microRNAs in neuronal development. Neural Dev. 5, 25.10.1186/1749-8104-5-25Suche 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.1972910Suche 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.Suche 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.0003148Suche 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.xSuche 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/gkj112Suche 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.xSuche 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.2006.03.043Suche in Google Scholar PubMed
Hebert, S.S. and De Strooper, B. (2007). Molecular biology. miRNAs in neurodegeneration. Science 317, 1179–1180.10.1126/science.1148530Suche 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.273.44.28625Suche 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.1062961Suche 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.2012.12.008Suche 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-r173Suche 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.1465Suche 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.1140481Suche 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/nmeth843Suche 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/gkq1027Suche 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.5980303Suche 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.2005-0441Suche in Google Scholar
Kulkarni, M., Ozgur, S., and Stoecklin, G. (2010). On track with P-bodies. Biochem. Soc. Trans. 38, 242–251.10.1042/BST0380242Suche 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.2146903Suche 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.01694-08Suche 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.Suche 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.1002242Suche 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.1065329Suche 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-YSuche 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/nature01957Suche 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)01018-3Suche 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.2010.08.002Suche 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/nature03315Suche 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.2008.278Suche 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.1076311Suche in Google Scholar PubMed
Maiorano, N.A. and Mallamaci, A. (2009). Promotion of embryonic cortico-cerebral neuronogenesis by miR-124. Neural Dev. 4, 40.10.1186/1749-8104-4-40Suche 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.2007.07.015Suche 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.20750Suche 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.2008.07.020Suche 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-r68Suche 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.0030215Suche 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.2013.125Suche 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.2010.08.074Suche 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, 98.10.1186/1471-2202-10-98Suche 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.5037-05.2006Suche 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.1999.9523Suche 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.2009.04.007Suche 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/nrn3234Suche 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.006Suche in Google Scholar PubMed
Rajasekharan, S. and Kennedy, T.E. (2009). The netrin protein family. Genome Biol. 10, 239.10.1186/gb-2009-10-9-239Suche 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.7601668Suche 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, 901–906.10.1038/35002607Suche 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)00863-2Suche 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, 707–722.10.2174/1566524011313050003Suche 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/nature05983Suche 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-10-2074Suche 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, 14.10.1186/1749-8104-8-14Suche 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.20070823Suche 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-r13Suche 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.7601923Suche 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.xSuche 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.2008-0319Suche 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.2006.10.016Suche 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.2008.04.033Suche 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.1399806Suche 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.1519107Suche 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.2006.07.006Suche 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.2005.07.070Suche 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.1114519Suche 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)90530-4Suche 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.25.21.9198-9208.2005Suche 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.2007.08.006Suche 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.2011.07.024Suche 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.1006432107Suche 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.1097434Suche 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/nature08139Suche 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.2008.06.002Suche 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.Suche 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)00541-5Suche 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.2010.04.017Suche 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.27.20130010Suche 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.1576Suche in Google Scholar PubMed PubMed Central
©2014 by De Gruyter
Artikel in diesem Heft
- Frontmatter
- Dopamine and reward seeking: the role of ventral tegmental area
- Fetal alcohol spectrum disorders and cognitive functions of young children
- Amyloid β in hereditary cerebral hemorrhage with amyloidosis-Dutch type
- Candidate biomarkers of multiple system atrophy in cerebrospinal fluid
- Role of neuroimaging in drug development
- MicroRNAs in central nervous system development
- Autonomic contributions in postural control: a review of the evidence
- The role of Toll-like receptors (TLRs) in stroke
- The role of Toll-like receptors in multiple sclerosis and possible targeting for therapeutic purposes
Artikel in diesem Heft
- Frontmatter
- Dopamine and reward seeking: the role of ventral tegmental area
- Fetal alcohol spectrum disorders and cognitive functions of young children
- Amyloid β in hereditary cerebral hemorrhage with amyloidosis-Dutch type
- Candidate biomarkers of multiple system atrophy in cerebrospinal fluid
- Role of neuroimaging in drug development
- MicroRNAs in central nervous system development
- Autonomic contributions in postural control: a review of the evidence
- The role of Toll-like receptors (TLRs) in stroke
- The role of Toll-like receptors in multiple sclerosis and possible targeting for therapeutic purposes