Regulation of miRNA expression during neural cell specification
Abstract
MicroRNA (miRNA) are a newly recognized class of small, noncoding RNA molecules that participate in the developmental control of gene expression. We have studied the regulation of a set of highly expressed neural miRNA during mouse brain development. Temporal control is a characteristic of miRNA regulation in C. elegans and Drosophila, and is also prominent in the embryonic brain. We observed significant differences in the onset and magnitude of induction for individual miRNAs. Comparing expression in cultures of embryonic neurons and astrocytes we found marked lineage specificity for each of the miRNA in our study. Two of the most highly expressed miRNA in adult brain were preferentially expressed in neurons (mir-124, mir-128). In contrast, mir-23, a miRNA previously implicated in neural specification, was restricted to astrocytes. mir-26 and mir-29 were more strongly expressed in astrocytes than neurons, others were more evenly distributed (mir-9, mir-125). Lineage specificity was further explored using reporter constructs for two miRNA of particular interest (mir-125 and mir-128). miRNA-mediated suppression of both reporters was observed after transfection of the reporters into neurons but not astrocytes. miRNA were strongly induced during neural differentiation of embryonic stem cells, suggesting the validity of the stem cell model for studying miRNA regulation in neural development.
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Decrease in miR-23 levels can lead to accumulation of Hes1 during retinal acid-induced neural differentiation in NT2 cells, which in turn affects neural differentiation.
“The decrease in miR-23 levels can lead to the accumulation of Hes1 during retinal acid-induced neural differentiation in NT2 cells, which in turn affects neural differentiation.”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [129]
miR-23 has the ability to affect neural differentiation.
“miR-23 has the ability to affect neural differentiation.”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [129]
Hes1 is also directly targeted by miR-124, and knockdown of miR-124 levels mediated by locked nucleic acids is similar to the effect of miR-23 inhibition.
“Hes1 is also directly targeted by miR-124, and the knockdown of miR-124 levels mediated by locked nucleic acids is similar to the effect of miR-23 inhibition.”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [129]
Regulation of neural development by miR-23 is probably achieved through the combined action of other miRNAs.
“It indicates that the regulation of neural development by miR-23 is probably achieved through the combined action of other miRNAs.”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [129]
Hes1 is an authentic target of miR-23.
“A basic helix-loop-helix transcriptional repressor, named Hes1, is an authentic target of miR-23.”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [129]
miR-23 is specifically expressed in astrocytes of the adult brain and is one of the miRNAs highly expressed in neurons during brain development.
“miR-23 is specifically expressed in astrocytes of the adult brain and is one of the miRNAs that are highly expressed in neurons during brain development.”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [129]
Expression level of Hes1 increases, ultimately hindering neuronal differentiation of P19 cells induced by retinoic acid.
“The expression level of Hes1 increases, ultimately hindering neuronal differentiation of P19 cells induced by the retinoic acid [[129], [130], [131]].”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [129]
Cites
Bartel (2004) · doi:10.1016/s0092-8674(04)00045-5 · Cited by 34,714 · see citing works
The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14
Lee, R. C., Feinbaum, R. L., & Ambros, V. (1993) · Cell · doi:10.1016/0092-8674(93)90529-y · Cited by 12,948 · see citing works
The functions of animal microRNAs
Ambros, V. (2004) · Nature · doi:10.1038/nature02871 · Cited by 10,728 · see citing works
MicroRNAs: small RNAs with a big role in gene regulation
He, L., & Hannon, G. J. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1379 · Cited by 6,992 · see citing works
Prediction of Mammalian MicroRNA Targets
Lewis, B. P., Shih, I., Jones-Rhoades, M. W., Bartel, D. P., & Burge, C. B. (2003) · Cell · doi:10.1016/s0092-8674(03)01018-3 · Cited by 5,098 · see citing works
Calin, G. A., Dumitru, C. D., Shimizu, M., Bichi, R., Zupo, S., Noch, E., Aldler, H., Rattan, S., Keating, M. J., Rai, K., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242606799 · Cited by 4,992 · see citing works
The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans
Reinhart, B. J., Slack, F. J., Basson, M., Pasquinelli, A. E., Bettinger, J. C., Rougvie, A. E., Horvitz, H. R., & Ruvkun, G. (2000) · Nature · doi:10.1038/35002607 · Cited by 4,989 · see citing works
Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers
Calin, G. A., Sevignani, C., Dumitru, C. D., Hyslop, T., Noch, E., Yendamuri, S., Shimizu, M., Rattan, S., Bullrich, F., Negrini, M., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307323101 · Cited by 4,096 · see citing works
John, B., Enright, A. J., Aravin, A., Tuschl, T., Sander, C., & Marks, D. S. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020363 · Cited by 3,796 · see citing works
MicroRNA targets in Drosophila
Enright, A. J., John, B., Gaul, U., Tuschl, T., Sander, C., & Marks, D. S. (2003) · Genome Biology · doi:10.1186/gb-2003-5-1-r1 · Cited by 3,597 · see citing works
Identification of Tissue-Specific MicroRNAs from Mouse
Lagos‐Quintana, M., Rauhut, R., Yalçın, A., Meyer, J., Lendeckel, W., & Tuschl, T. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00809-6 · Cited by 3,298 · see citing works
MicroRNAs Modulate Hematopoietic Lineage Differentiation
Chen, C.-Z., Li, L., Lodish, H. F., & Bartel, D. P. (2004) · Science · doi:10.1126/science.1091903 · Cited by 3,257 · see citing works
An Extensive Class of Small RNAs in Caenorhabditis elegans
Lee, R. C., & Ambros, V. (2001) · Science · doi:10.1126/science.1065329 · Cited by 2,828 · see citing works
Baulcombe, D. C. (2004) · Nature · doi:10.1038/nature02874 · Cited by 2,556 · see citing works
Brennecke, J., Hipfner, D. R., Stark, A., Russell, R. B., & Cohen, S. M. (2003) · Cell · doi:10.1016/s0092-8674(03)00231-9 · Cited by 2,031 · see citing works
Sempere, L. F., Freemantle, S. J., Pitha, I., Moss, E. G., Dmitrovsky, E., & Ambros, V. (2004) · Genome biology · doi:10.1186/gb-2004-5-3-r13 · Cited by 1,584 · see citing works
Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture
Ying, Q.-L., Stavridis, M., Griffiths, D., Li, M., & Smith, A. (2003) · Nature Biotechnology · doi:10.1038/nbt780 · Cited by 1,504 · see citing works
Lai, E. C. (2002) · Nature Genetics · doi:10.1038/ng865 · Cited by 1,478 · see citing works
MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias
Calin, G. A., Liu, C., Sevignani, C., Ferracin, M., Felli, N., Dumitru, C. D., Shimizu, M., Cimmino, A., Zupo, S., Dono, M., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404432101 · Cited by 1,279 · see citing works
Embryonic Stem Cell-Specific MicroRNAs
Houbaviy, H. B., Murray, M. F., & Sharp, P. A. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00227-2 · Cited by 1,131 · see citing works
miRNPs: a novel class of ribonucleoproteins containing numerous microRNAsPreprint
Mourelatos, Z., Dostie, J., Paushkin, S. V., Sharma, A. K., Charroux, B., Abel, L., Rappsilber, J., Mann, M., & Dreyfuss, G. (2002) · Genes & Development · doi:10.1101/gad.974702 · Cited by 1,081 · see citing works
A microRNA array reveals extensive regulation of microRNAs during brain development
Krichevsky, A. M., King, K. S., Donahue, C. P., Khrapko, K., & Kosik, K. S. (2003) · RNA · doi:10.1261/rna.5980303 · Cited by 1,040 · see citing works
The Drosophila MicroRNA Mir-14 Suppresses Cell Death and Is Required for Normal Fat Metabolism
Xu, P., Vernooy, S. Y., Guo, M., & Hay, B. A. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00250-1 · Cited by 1,006 · see citing works
Human embryonic stem cells express a unique set of microRNAs
Suh, M. R., Lee, Y., Kim, J. Y., Kim, S.-K., Moon, S., Lee, J. Y., Cha, K., Chung, H., Yoon, H. S., Moon, S. Y., et al. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.02.019 · Cited by 974 · see citing works
An oligonucleotide microchip for genome-wide microRNA profiling in human and mouse tissues
Liu, C., Calin, G. A., Meloon, B., Gamliel, N., Sevignani, C., Ferracin, M., Dumitru, C. D., Shimizu, M., Zupo, S., Dono, M., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403293101 · Cited by 947 · see citing works
Moss, E. G., Lee, R. C., & Ambros, V. (1997) · Cell · doi:10.1016/s0092-8674(00)81906-6 · Cited by 827 · see citing works
Identification of Drosophila MicroRNA Targets
Stark, A., Brennecke, J., Russell, R. B., & Cohen, S. M. (2003) · PLoS Biology · doi:10.1371/journal.pbio.0000060 · Cited by 784 · see citing works
A combined computational-experimental approach predicts human microRNA targetsPreprint
Kiriakidou, M., Nelson, P. T., Kouranov, A., Fitziev, P., Bouyioukos, C., Mourelatos, Z., & Hatzigeorgiou, A. G. (2004) · Genes & Development · doi:10.1101/gad.1184704 · Cited by 774 · see citing works
Alternative pre-mRNA splicing and proteome expansion in metazoans
Maniatis, T., & Tasic, B. (2002) · Nature · doi:10.1038/418236a · Cited by 768 · see citing works
A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans
Johnston, R. J., & Hobert, O. (2003) · Nature · doi:10.1038/nature02255 · Cited by 760 · see citing works
Slack, F. J., Basson, M., Liu, Z., Ambros, V., Horvitz, H. R., & Ruvkun, G. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80245-2 · Cited by 751 · see citing works
Isshiki, T., Pearson, B. J., Holbrook, S. D., & Doe, C. Q. (2001) · Cell · doi:10.1016/s0092-8674(01)00465-2 · Cited by 684 · see citing works
Identification of many microRNAs that copurify with polyribosomes in mammalian neurons
Kim, J., Krichevsky, A. M., Grad, Y. H., Hayes, G. D., Kosik, K. S., Church, G. M., & Ruvkun, G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2333854100 · Cited by 570 · see citing works
A Small Modulatory dsRNA Specifies the Fate of Adult Neural Stem Cells
Kuwabara, T., Hsieh, J., Nakashima, K., Taira, K., & Gage, F. H. (2004) · Cell · doi:10.1016/s0092-8674(04)00248-x · Cited by 442 · see citing works
Compartmentalized Synthesis and Degradation of Proteins in Neurons
Steward, O., & Schuman, E. M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00635-4 · Cited by 380 · see citing works
Numerous microRNPs in neuronal cells containing novel microRNAs
Dostie, J., MOURELATOS, Z., YANG, M., Sharma, A. K., & Dreyfuss, G. (2003) · RNA · doi:10.1261/rna.2141503 · Cited by 376 · see citing works
Abrahante, J. E., Daul, A. L., Li, M., Volk, M. L., Tennessen, J. M., Miller, E. A., & Rougvie, A. E. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00127-8 · Cited by 354 · see citing works
Lin, S.-Y., Johnson, S., Abraham, M. C., Vella, M. C., Pasquinelli, A. E., Gamberi, C., Gottlieb, E., & Slack, F. J. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00124-2 · Cited by 351 · see citing works
MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode
Chang, S. S., Johnston, R. J., Frøkjær‐Jensen, C., Lockery, S. R., & Hobert, O. (2004) · Nature · doi:10.1038/nature02752 · Cited by 346 · see citing works
Control of Developmental Timing by MicroRNAs and Their Targets
Pasquinelli, A. E., & Ruvkun, G. (2002) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.18.012502.105832 · Cited by 339 · see citing works
Defined Conditions for Neural Commitment and Differentiation
Ying, Q., & Smith, A. G. (2003) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(03)65023-8 · Cited by 328 · see citing works
Yang, H. Y., Roy, R., & Ambros, V. (1998) · Development · doi:10.1242/dev.125.18.3585 · Cited by 205 · see citing works
lin-14 regulates the timing of synaptic remodelling in Caenorhabditis elegans
Hallam, S., & Jin, Y. (1998) · Nature · doi:10.1038/25757 · Cited by 193 · see citing works
Seiler, A. E. M., Visan, A., Buesen, R., Genschow, E., & Spielmann, H. (2004) · Reproductive Toxicology · doi:10.1016/j.reprotox.2003.10.015 · Cited by 189 · see citing works
Self-citationBanerjee, D., & Slack, F. J. (2002) · BioEssays · doi:10.1002/bies.10046 · Cited by 166 · see citing works
Control of developmental timing in animals
Rougvie, A. E. (2001) · Nature Reviews Genetics · doi:10.1038/35088566 · Cited by 138 · see citing works
Musunuru, K., & Darnell, R. B. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.239 · Cited by 107 · see citing works
Drejer, J., Larsson, O. M., Kvamme, E., Svenneby, G., Hertz, L., & Schousboe, A. (1985) · Neurochemical Research · doi:10.1007/bf00964771 · Cited by 101 · see citing works
Euling, S. Y., & Ambros, V. (1996) · Cell · doi:10.1016/s0092-8674(00)81045-4 · Cited by 100 · see citing works
Tiedge, H., Bloom, F. E., & Richter, D. (1999) · Science · doi:10.1126/science.283.5399.186 · Cited by 89 · see citing works
Why do miRNAs live in the miRNP?Preprint
Schwarz, D. S., & Zamore, P. D. (2002) · Genes & Development · doi:10.1101/gad.992502 · Cited by 88 · see citing works
P19 Embryonal Carcinoma Cells: A Source of Cultured Neurons Amenable to Genetic Manipulation
MacPherson, P. A., & McBurney, M. W. (1995) · Methods · doi:10.1006/meth.1995.1029 · Cited by 60 · see citing works
Neuronal differentiation of P19 embryonal carcinoma cells in defined media
Yao, M., Bain, G., & Gottlieb, D. I. (1995) · Journal of Neuroscience Research · doi:10.1002/jnr.490410610 · Cited by 54 · see citing works
Yang, H. Y., Lee, R. C., & Ambros, V. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.6.2285-2295.2000 · Cited by 54 · see citing works
Kawasaki, H., & Taira, K. (2003) · Nucleic Acids Symposium Series · doi:10.1093/nass/3.1.243 · Cited by 31 · see citing works
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Oncomirs — microRNAs with a role in cancer
Esquela‐Kerscher, A., & Slack, F. J. (2006) · Nature reviews. Cancer · doi:10.1038/nrc1840 · Cited by 7,038 · see citing works
Makeyev, E. V., Zhang, J., Carrasco, M. A., & Maniatis, T. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.07.015 · Cited by 1,395 · see citing works
Hébert, S. S., Horré, K., Nicolaï, L., Papadopoulou, A. S., Mandemakers, W., Silahtaroglu, A. N., Kauppinen, S., Delacourte, A., & De Strooper, B. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710263105 · Cited by 1,183 · see citing works
MicroRNAs in Development and Disease
Sayed, D. H., & Abdellatif, M. (2011) · Physiological Reviews · doi:10.1152/physrev.00006.2010 · Cited by 1,074 · see citing works
miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche
Cheng, L.-C., Pastrana, É., Tavazoie, M. F., & Doetsch, F. K. (2009) · Nature Neuroscience · doi:10.1038/nn.2294 · Cited by 976 · see citing works
Silber, J., Lim, D. A., Petritsch, C. K., Persson, A. I., Maunakea, A. K., Yu, M., VandenBerg, S. R., Ginzinger, D. G., James, C. D., Costello, J., et al. (2008) · BMC Medicine · doi:10.1186/1741-7015-6-14 · Cited by 940 · see citing works
Thum, T., Galuppo, P., Wolf, C., Fiedler, J., Kneitz, S., Laake, L. W. V., Doevendans, P. A., Mummery, C. L., Borlak, J. T., Haverich, A., et al. (2007) · Circulation · doi:10.1161/circulationaha.107.687947 · Cited by 890 · see citing works
Cheng, L., Sharples, R. A., Scicluna, B. J., & Hill, A. F. (2014) · Journal of Extracellular Vesicles · doi:10.3402/jev.v3.23743 · Cited by 840 · see citing works
Kosik, K. S. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn2037 · Cited by 827 · see citing works
Rybak‐Wolf, A., Fuchs, H. R., Smirnova, L., Brandt, C., Pohl, E. E., Nitsch, R., & Wulczyn, F. G. (2008) · Nature Cell Biology · doi:10.1038/ncb1759 · Cited by 788 · see citing works
Self-citationPonomarev, E. D., Veremeyko, T., Barteneva, N., Krichevsky, A. M., & Weiner, H. L. (2011) · Nature Medicine · doi:10.1038/nm.2266 · Cited by 787 · see citing works
An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration
Lehmann, S. M., Krüger, C., Park, B., Derkow, K., Rosenberger, K., Baumgart, J., Trimbuch, T., Eom, G. D., Hinz, M., Kaul, D., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3113 · Cited by 780 · see citing works
Self-citationFelli, N., Fontana, L., Pelosi, E., Botta, R., Bonci, D., Facchiano, F., Liuzzi, F., Lulli, V., Morsilli, O., Santoro, S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506216102 · Cited by 760 · see citing works
MicroRNAs: key regulators of stem cells
Gangaraju, V. K., & Lin, H. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2621 · Cited by 731 · see citing works
Reciprocal actions of REST and a microRNA promote neuronal identity
Conaco, C., Otto, S. J., Han, J.-J., & Mandel, G. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511041103 · Cited by 714 · see citing works
Godlewski, J. A., Nowicki, M. O., Bronisz, A., Williams, S. P., Otsuki, A., Nuovo, G. J., Ray‐Chaudhury, A., Newton, H. B., Chiocca, E. A., & Lawler, S. E. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-2629 · Cited by 702 · see citing works
Specific MicroRNAs Modulate Embryonic Stem Cell–Derived Neurogenesis
Krichevsky, A. M., Sonntag, K., Ole Isacson, A., & Kosik, K. S. (2005) · Stem Cells · doi:10.1634/stemcells.2005-0441 · Cited by 680 · see citing works
Micro-RNA speciation in fetal, adult and Alzheimer's disease hippocampus
Lukiw, W. J. (2007) · Neuroreport · doi:10.1097/wnr.0b013e3280148e8b · Cited by 666 · see citing works
Biological functions of microRNAs: a review
Huang, Y., Shen, X. J., Zou, Q., Wang, S. P., Tang, S. M., & Zhang, G. Z. (2010) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-010-0050-6 · Cited by 650 · see citing works
Brites, D., & Fernandes, A. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00476 · Cited by 599 · see citing works
“Previous studies indicate that miR-124 and miR-128 are primarily expressed in neurons, whereas miR-23, miR-26, and miR-29 exist in large amount in astrocytes, supporting a differential nature of expression (Smirnova et al., 2005).”
BackgroundThe Role of MicroRNAs in Human Diseases.
Ardekani, A. M., & Naeini, M. M. (2010) · Europe PMC (PubMed Central) · Cited by 552 · see citing works
Babenko, O., Kovalchuk, I., & Metz, G. A. S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.013 · Cited by 513 · see citing works
Cerebellar neurodegeneration in the absence of microRNAs
Schaefer, A., O’Carroll, D., Tan, C. L., Hillman, D. E., Sugimori, M., Llinás, R., & Greengard, P. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070823 · Cited by 484 · see citing works
MicroRNA expression in the adult mouse central nervous system
Bak, M., Silahtaroglu, A., Møller, M., Christensen, M., Rath, M. F., Skryabin, B. V., Tommerup, N., & Kauppinen, S. (2008) · RNA · doi:10.1261/rna.783108 · Cited by 463 · see citing works
Alterations of the microRNA network cause neurodegenerative disease
Hébert, S. S., & De Strooper, B. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2008.12.003 · Cited by 452 · see citing works
MicroRNA regulation of Alzheimer's Amyloid precursor protein expression
Hébert, S. S., Horré, K., Nicolaï, L., Bergmans, B., Papadopoulou, A. S., Delacourte, A., & De Strooper, B. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.11.009 · Cited by 436 · see citing works
NONCODING RNAS IN THE MAMMALIAN CENTRAL NERVOUS SYSTEM
Cao, X., Yeo, G. W.-M., Muotri, A. R., Kuwabara, T., & Gage, F. H. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112839 · Cited by 432 · see citing works
MicroRNAs in neuronal function and dysfunction
Im, H.-I., & Kenny, P. J. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.01.004 · Cited by 399 · see citing works
Kapsimali, M., Kloosterman, W. P., de Bruijn, E., Rosa, F., Plasterk, R. H. A., & Wilson, S. W. (2007) · Genome biology · doi:10.1186/gb-2007-8-8-r173 · Cited by 376 · see citing works
A microRNA-based gene dysregulation pathway in Huntington's disease
Johnson, R., Zuccato, C., Belyaev, N. D., Guest, D. J., Cattaneo, E. F., & Buckley, N. J. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.11.001 · Cited by 360 · see citing works
De Pietri Tonelli, D., Pulvers, J. N., Haffner, C., Murchison, E. P., Hannon, G. J., & Huttner, W. B. (2008) · Development · doi:10.1242/dev.025080 · Cited by 343 · see citing works
MicroRNAs (miRNAs) in Neurodegenerative Diseases
Nelson, P. T., Wang, W., & Rajeev, B. W. (2008) · Brain Pathology · doi:10.1111/j.1750-3639.2007.00120.x · Cited by 325 · see citing works
MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation
Yu, J., Chung, K.-H., Deo, M., Thompson, R. C., & Turner, D. L. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.06.002 · Cited by 312 · see citing works
Retracted: Post‐transcriptional regulation of the let‐7 microRNA during neural cell specification
Wulczyn, F. G., Smirnova, L., Rybak‐Wolf, A., Brandt, C., Kwidzinski, E., Ninnemann, O., Strehle, M., Seiler, A. E. M., Schumacher, S., & Nitsch, R. (2006) · The FASEB Journal · doi:10.1096/fj.06-6130com · Cited by 312 · see citing works
Self-citationRetractedFactors controlling permeability of the blood–brain barrier
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MicroRNAs in Alzheimer’s Disease
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MicroRNA, mRNA, and protein expression link development and aging in human and macaque brainPreprint
Somel, M., Guo, S., Fu, N., Zheng, Y., Hu, H., Xu, Y., Yuan, Y., Ning, Z., Hu, Y., Menzel, C., et al. (2010) · Genome Research · doi:10.1101/gr.106849.110 · Cited by 296 · see citing works
Bruno, I., Karam, R., Huang, L., Bhardwaj, A., Lou, C. H., Shum, E. Y., Song, H.-W., Corbett, M. A., Gifford, W. D., Gécz, J., et al. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.04.018 · Cited by 295 · see citing works
Mehler, M. F., & Mattick, J. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00036.2006 · Cited by 294 · see citing works
MicroRNA profiling in human medulloblastoma
Ferretti, E., Smaele, E. D., Pò, A., Marcotullio, L. D., Tosi, E., Espinola, M. S. B., Rocco, C. D., Riccardi, R., Giangaspero, F., Farcomeni, A., et al. (2008) · International Journal of Cancer · doi:10.1002/ijc.23948 · Cited by 293 · see citing works
MicroRNA-125b Promotes Neuronal Differentiation in Human Cells by Repressing Multiple Targets
Le, M. T. N., Xie, H., Zhou, B., Chia, P. H., Rizk, P., Um, M., Udolph, G., Yang, H. H., Lim, B., & Lodish, H. F. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01694-08 · Cited by 288 · see citing works
MicroRNA signatures of TRAIL resistance in human non-small cell lung cancer
Garofalo, M., Quintavalle, C., Leva, G. D., Zanca, C., Romano, G., Taccioli, C., Liu, C. G., Croce, C. M., & Condorelli, G. (2008) · Oncogene · doi:10.1038/onc.2008.6 · Cited by 290 · see citing works
Detection of mammalian microRNA expression by in situ hybridization with RNA oligonucleotides
Deo, M., Yu, J., Chung, K.-H., Tippens, M., & Turner, D. L. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20847 · Cited by 283 · see citing works
Moreau, M., Bruse, S., David-Rus, R., Buyske, S. G., & Brzustowicz, L. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.039 · Cited by 278 · see citing works
The emerging roles of microRNAs in CNS injuries
Bhalala, O. G., Srikanth, M., & Kessler, J. A. (2013) · Nature Reviews Neurology · doi:10.1038/nrneurol.2013.67 · Cited by 274 · see citing works
The miR-17 ∼ 92 cluster collaborates with the Sonic Hedgehog pathway in medulloblastoma
Uziel, T., Karginov, F. V., Xie, S., Parker, J. S., Wang, Y., Gajjar, A. J., He, L., Ellison, D. W., Gilbertson, R. J., Hannon, G. J., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809579106 · Cited by 275 · see citing works
Zhang, Y., Yan, L., Wu, Q.-N., Du, Z.-M., Chen, J., Liao, D.-Z., Huang, M., Hou, J.-H., Wu, Q., Zeng, M., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-2435 · Cited by 273 · see citing works
MicroRNA profile analysis of human prostate cancers
Tong, A. W., Fulgham, P. F., Jay, C. M., Chen, P., Khalil, I. G., Liu, S., Senzer, N. N., Eklund, A. C., Han, J., & Nemunaitis, J. J. (2008) · Cancer Gene Therapy · doi:10.1038/cgt.2008.77 · Cited by 271 · see citing works
Mellios, N., Huang, H., Grigorenko, A. P., Rogaev, E. I., & Akbarian, S. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn201 · Cited by 270 · see citing works
Expression of microRNAs and their precursors in synaptic fractions of adult mouse forebrain
Lugli, G., Torvik, V. I., Larson, J., & Smalheiser, N. R. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05413.x · Cited by 261 · see citing works
Vreugdenhil, E., Veríssimo, C. S., Mariman, R., Kamphorst, J. T., Barbosa, J. S., Zweers, T. J., Champagne, D. L., Schouten, T. G., Meijer, O. C., de Kloet, E. R., et al. (2009) · Endocrinology · doi:10.1210/en.2008-1335 · Cited by 259 · see citing works
Wu, J., & Xie, X. S. (2006) · Genome biology · doi:10.1186/gb-2006-7-9-r85 · Cited by 259 · see citing works
Identification of Dynamically Regulated MicroRNA and mRNA Networks in Developing Oligodendrocytes
Lau, P., Verrier, J. D., Nielsen, J. A., Johnson, K. R., Notterpek, L. M., & Hudson, L. D. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1932-08.2008 · Cited by 254 · see citing works
miR-124 Inhibits STAT3 Signaling to Enhance T Cell–Mediated Immune Clearance of Glioma
Wei, J., Wang, F., Kong, L.-Y., Xu, S., Doucette, T. A., Ferguson, S. D., Yang, Y., McEnery, K., Jethwa, K. R., Gjyshi, O., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-4318 · Cited by 253 · see citing works
Jovičić, A., Roshan, R., Moisoi, N., Pradervand, S., Moser, R., Pillai, B., & Luthi-Carter, R. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.0600-12.2013 · Cited by 251 · see citing works
The involvement of microRNAs in neurodegenerative diseases
Maciotta, S., Meregalli, M., & Torrente, Y. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00265 · Cited by 247 · see citing works
Tay, Y., Tam, W. L., Ang, Y.-S., Gaughwin, P. M., Yang, H. H., Wang, W., Liu, R., George, J., Ng, H., Perera, R. J., et al. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0295 · Cited by 236 · see citing works
Hwang, D. W., Son, S., Jang, J., Youn, H., Lee, S., Lee, D., Lee, Y., Jeong, J. M., Kim, W. J., & Lee, D. S. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.03.047 · Cited by 234 · see citing works
Guo, L., & Lu, Z. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011387 · Cited by 233 · see citing works
Lee, C.-T., Risom, T., & Strauss, W. M. (2007) · DNA and Cell Biology · doi:10.1089/dna.2006.0545 · Cited by 233 · see citing works
Rybak, A., Fuchs, H., Hadian, K., Smirnova, L., Wulczyn, E. A., Michel, G., Nitsch, R., Krappmann, D., & Wulczyn, F. (2009) · Nature Cell Biology · doi:10.1038/ncb1987 · Cited by 262 · see citing works
Self-citationDecreased expression of miR‐125b and miR‐100 in oral cancer cells contributes to malignancy
Henson, B. J., Bhattacharjee, S., O’Dee, D. M., Feingold, E., & Gollin, S. M. (2009) · Genes Chromosomes and Cancer · doi:10.1002/gcc.20666 · Cited by 228 · see citing works
Microglia secrete miR-146a-5p-containing exosomes to regulate neurogenesis in depression
Fan, C., Li, Y., Lan, T., Wang, W., Long, Y., & Yu, S. Y. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2021.11.006 · Cited by 227 · see citing works
Saugstad, J. A. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2010.101 · Cited by 225 · see citing works
An updated role of microRNA-124 in central nervous system disorders: a review
Sun, Y., Luo, Z.-M., Guo, X.-M., Su, D.-F., & Liu, X. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00193 · Cited by 223 · see citing works
Regulation of prelamin A but not lamin C by miR-9, a brain-specific microRNA
Jung, H.-J., Coffinier, C., Choe, Y., Beigneux, A. P., Davies, B. S. J., Yang, S. H., Barnes, R. H., Hong, J., Sun, T., Pleasure, S. J., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111780109 · Cited by 221 · see citing works
Transcriptome-wide Discovery of microRNA Binding Sites in Human Brain
Boudreau, R. L., Jiang, P., Gilmore, B. L., Spengler, R. M., Tirabassi, R. S., Nelson, J. A., Ross, C. A., Xing, Y., & Davidson, B. L. (2014) · Neuron · doi:10.1016/j.neuron.2013.10.062 · Cited by 217 · see citing works
Bottoni, A., Zatelli, M. C., Ferracin, M., Tagliati, F., Piccin, D., Vignali, C., Calin, G. A., Negrini, M., Croce, C. M., & Uberti, E. C. D. (2006) · Journal of Cellular Physiology · doi:10.1002/jcp.20832 · Cited by 219 · see citing works
MicroRNA: Implications for Alzheimer Disease and other Human CNS Disorders
Maes, O. C., Chertkow, H. M., Wang, E., & Schipper, H. M. (2009) · Current Genomics · doi:10.2174/138920209788185252 · Cited by 216 · see citing works
Fang, M., Wang, J., Zhang, X., Geng, Y., Hu, Z., Rudd, J. A., Ling, S., Chen, W., & Han, S. (2011) · Toxicology Letters · doi:10.1016/j.toxlet.2011.11.032 · Cited by 215 · see citing works
Schlesinger, J., Schueler, M., Grunert, M., Fischer, J. J., Zhang, Q., Krueger, T., Lange, M., Tönjes, M., Dunkel, I., & Sperling, S. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001313 · Cited by 214 · see citing works
Adlakha, Y. K., & Saini, N. (2014) · Molecular Cancer · doi:10.1186/1476-4598-13-33 · Cited by 213 · see citing works
Lukiw, W. J., & Pogue, A. I. (2007) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2007.06.004 · Cited by 208 · see citing works
Hu, G., Yao, H., Chaudhuri, A. D., Duan, M., Yelamanchili, S. V., Wen, H., Cheney, P. D., Fox, H. S., & Buch, S. J. (2012) · Cell Death and Disease · doi:10.1038/cddis.2012.114 · Cited by 204 · see citing works
Alterations of Serum Levels of BDNF-Related miRNAs in Patients with Depression
Li, Y., Xu, M., Zong-hua, G., Wang, Y., Yue, Z., Zhang, Y.-X., Li, X., Zhang, C. M., Xie, S., & Wang, P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063648 · Cited by 204 · see citing works
MicroRNA function in neuronal development, plasticity and disease
Fiore, R., Siegel, G., & Schratt, G. M. (2007) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2007.12.006 · Cited by 201 · see citing works
Identification of MicroRNA-124-3p as a Putative Epigenetic Signature of Major Depressive Disorder
Roy, B., Dunbar, M., Shelton, R. C., & Dwivedi, Y. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.175 · Cited by 199 · see citing works
Therapeutic potential for microRNAs
Esau, C., & Monia, B. P. (2007) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2007.03.007 · Cited by 196 · see citing works
Identification and Characterization of MicroRNAs Expressed in the Mouse Eye
Karali, M., Peluso, I., Marigo, V., & Banfi, S. (2007) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.06-0866 · Cited by 195 · see citing works
The Role of MicroRNAs in Biological Processes
Tüfekçi, K. U., Meuwissen, R. L. J., & Genç, Ş. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-748-8_2 · Cited by 195 · see citing works
Vieira, M. S., Santos, A. K., Vasconcellos, R., Goulart, V. A. M., Parreira, R. C., Kihara, A. H., Ulrich, H., & Resende, R. R. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2018.08.002 · Cited by 191 · see citing works
Shi, Y., Sun, G., Zhao, C., & Stewart, R. (2007) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2007.06.004 · Cited by 188 · see citing works
MicroRNA-9 Modulates Hes1 Ultradian Oscillations by Forming a Double-Negative Feedback Loop
Bonev, B., Stanley, P., & Papalopulu, N. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.05.017 · Cited by 186 · see citing works
MicroRNAs in Alzheimer's disease
Delay, C., Mandemakers, W., & Hébert, S. S. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.01.003 · Cited by 185 · see citing works
Epigenetic mechanisms of major depression: Targeting neuronal plasticity
Uchida, S., Yamagata, H., Seki, T., & Watanabe, Y. (2018) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12621 · Cited by 181 · see citing works
Roles of small regulatory RNAs in determining neuronal identity
Li, X., & Jin, P. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2739 · Cited by 180 · see citing works
Cougot, N., Bhattacharyya, S. N., Tapia-Arancibia, L., Bordonné, R., Filipowicz, W., Bertrand, É., & Rage, F. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4155-08.2008 · Cited by 178 · see citing works
MicroRNAs: Small molecules with big roles in neurodevelopment and diseases
Sun, E., & Shi, Y. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.08.005 · Cited by 178 · see citing works
Yuva-Aydemir, Y., Simkin, A., Gascon, E., & Gao, F. (2011) · RNA Biology · doi:10.4161/rna.8.4.16019 · Cited by 177 · see citing works
Vallelunga, A., Ragusa, M., Mauro, S. D., Iannitti, T., Pilleri, M., Biundo, R., Weis, L., Pietro, C. D., Iuliis, A. D., Nicoletti, A. S. Q., et al. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00156 · Cited by 175 · see citing works
Lou, C. H., Shao, A., Shum, E. Y., Espinoza, J. L., Huang, L., Karam, R., & Wilkinson, M. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.01.028 · Cited by 175 · see citing works
Nissan, X., Blondel, S., Navarro, C. L., Maury, Y., Denis, C., Girard, M., Martinat, C., Sandre‐Giovannoli, A. D., Lévy, N., & Peschanski, M. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.05.015 · Cited by 168 · see citing works
Sheinerman, K. S., & Umansky, S. R. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00150 · Cited by 171 · see citing works
Emerging role of microRNAs in major depressive disorder: diagnosis and therapeutic implications
Dwivedi, Y. (2014) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2014.16.1/ydwivedi · Cited by 169 · see citing works
MicroRNAs in Neurodegenerative Diseases
(2017) · International Review of Cell and Molecular Biology · doi:10.1016/bs.ircmb.2017.04.002 · Cited by 168 · see citing works
The role of microRNAs in the regulation of cancer stem cells
Takahashi, R., Miyazaki, H., & Ochiya, T. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2013.00295 · Cited by 167 · see citing works
Micro RNA-125b (miRNA-125b) function in astrogliosis and glial cell proliferation
Pogue, A. I., Cui, J. G., Li, Y. Y., Zhao, Y., Culicchia, F., & Lukiw, W. J. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.03.054 · Cited by 165 · see citing works
Laneve, P., Marcotullio, L. D., Gioia, U., Fiori, M. E., Ferretti, E., Gulino, A., Bozzoni, I., & Caffarelli, E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700071104 · Cited by 165 · see citing works
The roles of amyloid precursor protein (APP) in neurogenesis
Zhou, Z., Chan, C. H.-S., Ma, Q., Xu, X., Xiao, Z., & Tan, E. (2011) · Cell Adhesion & Migration · doi:10.4161/cam.5.4.16986 · Cited by 169 · see citing works
MicroRNAs and endocrine biology
Cuellar, T. L., & McManus, M. T. (2005) · Journal of Endocrinology · doi:10.1677/joe.1.06426 · Cited by 160 · see citing works
- Authors
- Smirnova, L., Gräfe, A., Seiler, A., Schumacher, S., Nitsch, R., & Wulczyn, F. G.
- Affiliations
- Charité – Universitätsmedizin Berlin (DE)
- German Federal Institute for Risk Assessment (BfR) (DE)
- Corresponding author
- Wulczyn, F. Gregory
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2005-03
- Volume
- 21
- Issue
- 6
- Pages
- 1469-1477
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2116641097
- Cited by
- 707
- References
- 55
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 13 · 2023: 23 · 2022: 22 · 2021: 34 · 2020: 27 · 2019: 29 · 2018: 30 · 2017: 20 · 2016: 37 · 2015: 51 · 2014: 50 · 2013: 52 · 2012: 54
- FWCI
- 11.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- OpenAgrar (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- microRNA, brain development, miRNA expression regulation, astrocytes, embryonic neurons, miR-124, miR-128, miR-125, miR-23, miR-26, miR-29, miR-9, embryonic stem cell differentiation, temporal gene expression
- MeSH terms
- Animals, Animals, Newborn, Cell Differentiation, Cell Line, Neurons, Stem Cells, Gene Expression Regulation, Developmental, MicroRNAs, Mice
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