The DOI matches its Crossref record; 55 of the 55 references it cites were found in a registry or an index.
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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In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“Notably, three miRNAs (miR-23, miR-26 and miR-29) that are found in oligodendrocyte lineage cells were previously described as enriched in astrocytes (Smirnova et al., 2005).”
From Identification of Dynamically Regulated MicroRNA and mRNA Networks in Developing Oligodendrocytes (2008) · cites this paper as Smirnova et al., 2005
In the citing paper
“miR-124 is known to be expressed in the CNS by neuronal cells23,39–41.”
From MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-α–PU.1 pathway (2011) · cites this paper as [23]
In the citing paper
“Such expression in neurons of the adult brain is shared with mouse miR-124 [30].”
From MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system (2007) · cites this paper as [30]
In the citing paper
“This profile is one of the best conserved miRNA patterns, as a similar restriction to mature neurons is seen for mouse and fly miR-124 [12,30].”
From MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system (2007) · cites this paper as [30]
In the citing paper
“miR-23 is involved in neuronal specification, and miR-146a implicated in the prevention of neuroligin 1-dependent synaptogenesis, and both were enriched in astrocytes compared to neurons [54, 67].”
From Differential RNA packaging into small extracellular vesicles by neurons and astrocytes (2021) · cites this paper as [67]
In the citing paper
“being prominently observed in differentiating neuronal cells29,31”
From MiR-128-3p – a gray eminence of the human central nervous system (2024) · cites this paper as [31]
Citations
Cites
Bartel (2004) · doi:10.1016/s0092-8674(04)00045-5 · Cited by 34,714
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
The functions of animal microRNAs
Ambros, V. (2004) · Nature · doi:10.1038/nature02871 · Cited by 10,728
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 7,118
Prediction of Mammalian MicroRNA Targets
Lewis, B. P., Shih, I.-H., Jones-Rhoades, M. W., Bartel, D. P., & Burge, C. B. (2003) · Cell · doi:10.1016/s0092-8674(03)01018-3 · Cited by 5,199
Calin, G. A., Dumitru, C. D., Shimizu, M., Bichi, R., Zupo, S., Noch, E., Aldler, H., Rattan, S., Keating, M., Rai, K., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242606799 · Cited by 5,111
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
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
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
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
Identification of tissue-specific microRNAs from mouse
Lagos-Quintana, M., Rauhut, R., Yalcin, A., Meyer, J., Lendeckel, W., & Tuschl, T. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00809-6 · Cited by 3,355
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
An Extensive Class of Small RNAs in Caenorhabditis elegans
Lee, R. C., & Ambros, V. (2001) · Science · doi:10.1126/science.1065329 · Cited by 2,922
Baulcombe, D. C. (2004) · Nature · doi:10.1038/nature02874 · Cited by 2,556
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 2,042
Sempere, L. F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., & Ambros, V. (2004) · Genome Biology · doi:10.1186/gb-2004-5-3-r13 · Cited by 1,578
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
Lai, E. C. (2002) · Nature Genetics · doi:10.1038/ng865 · Cited by 1,487
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
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 1,142
miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs
Mourelatos, Z., Dostie, J., Paushkin, S., Sharma, A., Charroux, B., Abel, L., Rappsilber, J., Mann, M., & Dreyfuss, G. (2002) · Genes & Development · doi:10.1101/gad.974702 · Cited by 1,105
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
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 1,011
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
An oligonucleotide microchip for genome-wide microRNA profiling in human and mouse tissues
Liu, C.-G., 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 948
Moss, E. G., Lee, R. C., & Ambros, V. (1997) · Cell · doi:10.1016/s0092-8674(00)81906-6 · Cited by 850
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
Alternative pre-mRNA splicing and proteome expansion in metazoans
Maniatis, T., & Tasic, B. (2002) · Nature · doi:10.1038/418236a · Cited by 774
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
A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans
Johnston, R. J., & Hobert, O. (2003) · Nature · doi:10.1038/nature02255 · Cited by 760
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
Isshiki, T., Pearson, B. J., Holbrook, S. D., & Doe, C. Q. (2001) · Cell · doi:10.1016/s0092-8674(01)00465-2 · Cited by 684
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 586
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 447
Numerous microRNPs in neuronal cells containing novel microRNAs
DOSTIE, J., MOURELATOS, Z., YANG, M., SHARMA, A., & DREYFUSS, G. (2003) · RNA · doi:10.1261/rna.2141503 · Cited by 378
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 377
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 357
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 349
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 346
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 341
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
Yang, H. Y., Roy, R., & Ambros, V. (1998) · Development · doi:10.1242/dev.125.18.3585 · Cited by 205
lin-14 regulates the timing of synaptic remodelling in Caenorhabditis elegans
Hallam, S., & Jin, Y. (1998) · Nature · doi:10.1038/25757 · Cited by 193
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
Self-citationBanerjee, D., & Slack, F. J. (2002) · BioEssays · doi:10.1002/bies.10046 · Cited by 166
Control of developmental timing in animals
Rougvie, A. E. (2001) · Nature Reviews Genetics · doi:10.1038/35088566 · Cited by 137
Musunuru, K., & Darnell, R. B. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.239 · Cited by 109
Drejer, J., Larsson, O. M., Kvamme, E., Svenneby, G., Hertz, L., & Schousboe, A. (1985) · Neurochemical Research · doi:10.1007/bf00964771 · Cited by 101
Euling, S. Y., & Ambros, V. (1996) · Cell · doi:10.1016/s0092-8674(00)81045-4 · Cited by 100
Tiedge, H., Bloom, F. E., & Richter, D. (1999) · Science · doi:10.1126/science.283.5399.186 · Cited by 89
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
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
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
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
Kawasaki, H., & Taira, K. (2003) · Nucleic Acids Symposium Series · doi:10.1093/nass/3.1.243 · Cited by 31
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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
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
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Sayed, D. H., & Abdellatif, M. (2011) · Physiological Reviews · doi:10.1152/physrev.00006.2010 · Cited by 1,101
miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche
Cheng, L.-C., Pastrana, E., Tavazoie, M., & Doetsch, F. (2009) · Nature Neuroscience · doi:10.1038/nn.2294 · Cited by 1,001
Metadata
- 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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