A Mammalian microRNA Expression Atlas Based on Small RNA Library Sequencing
Open accessAbstract
MicroRNAs (miRNAs) are small noncoding regulatory RNAs that reduce stability and/or translation of fully or partially sequence-complementary target mRNAs. In order to identify miRNAs and to assess their expression patterns, we sequenced over 250 small RNA libraries from 26 different organ systems and cell types of human and rodents that were enriched in neuronal as well as normal and malignant hematopoietic cells and tissues. We present expression profiles derived from clone count data and provide computational tools for their analysis. Unexpectedly, a relatively small set of miRNAs, many of which are ubiquitously expressed, account for most of the differences in miRNA profiles between cell lineages and tissues. This broad survey also provides detailed and accurate information about mature sequences, precursors, genome locations, maturation processes, inferred transcriptional units, and conservation patterns. We also propose a subclassification scheme for miRNAs for assisting future experimental and computational functional analyses.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
miR-27a/b are expressed in SN of human midbrain.
“miR-27a/b are expressed in SN of human midbrain (Additional file 2a) [34–36]”
From miR-27a and miR-27b regulate autophagic clearance of damaged mitochondria by targeting PTEN-induced putative kinase 1 (PINK1) (2016) · cites this paper as [34]
miR-27a/b are expressed in human midbrain.
“Several previous studies showed that miR-27a/b are expressed in human midbrain [34–36].”
From miR-27a and miR-27b regulate autophagic clearance of damaged mitochondria by targeting PTEN-induced putative kinase 1 (PINK1) (2016) · cites this paper as [34]
Only a small population of miRNAs accounts for a majority of miRNA pool in the brain.
“Previous studies have shown that only a small population of miRNAs accounts for a majority of miRNA pool in the brain (Shin et al. 2010, Hu et al. 2011, Landgraf et al. 2007, Berezikov et al. 2006).”
From miR‐186 is decreased in aged brain and suppresses <scp>BACE</scp>1 expression (2016) · cites this paper as Landgraf et al. 2007
miRNAs often show strong cell type- and tissue-specific regulation of their targets.
“miRNAs often show strong cell typeand tissue-specific regulation of their targets (Landgraf et al., 2007;Jovic ˇic ´et al., 2013).”
From microRNA-33 Regulates ApoE Lipidation and Amyloid-β Metabolism in the Brain (2015) · cites this paper as Landgraf et al., 2007
miRNAs often show cell-type, tissue, and species-specific regulation of their target genes.
“Importantly, miRNAs quite often show cell-type, tissue, and species-specific regulation of their target genes due to the differences in their expression levels and the complexity of interaction with their targets in different cellular contexts (Landgraf et al., 2007;Jovic ˇic ´et al., 2013).”
From microRNA-33 Regulates ApoE Lipidation and Amyloid-β Metabolism in the Brain (2015) · cites this paper as Landgraf et al., 2007
miR-21 is significantly elevated in glioblastoma (GBM) and in many other tumors of various origins.
“Substantial data indicate that microRNA 21 (miR-21) is significantly elevated in glioblastoma (GBM) and in many other tumors of various origins.”
From MicroRNA 21 Promotes Glioma Invasion by Targeting Matrix Metalloproteinase Regulators (2008) · cites this paper as [33]
20 miRNAs are up-regulated more than 2-fold during oligodendrocyte differentiation, including miR-21, miR-152, miR-142-5p and -3p, miR-338, miR-339 and miR-378.
“We also found 20 miRNAs that are up-regulated more than 2 fold during differentiation and some were previously identified from rat brain tissues: miR-21, miR-152, miR-142-5p and -3p, miR-338, miR-339 and miR-378 (Landgraf et al., 2007).”
From Identification of Dynamically Regulated MicroRNA and mRNA Networks in Developing Oligodendrocytes (2008) · cites this paper as Landgraf et al., 2007
The 20 oligodendrocyte-enriched miRs included hsa-miR-219a, hsa-miR-338, and hsa-miR-23.
“Notably, these included hsa-miR-219a and hsa-miR-338, both known to promote myelin repair 54 , and hsa-miR-23, which enhances oligodendrocyte differentiation and myelin synthesis 55 .”
From Human brain microRNAs exhibit cell-type specificity and age dependence (2026) · cites this paper as [54]
hsa-miR-219a and hsa-miR-338 are known to promote myelin repair, and hsa-miR-23 enhances oligodendrocyte differentiation and myelin synthesis.
“both known to promote myelin repair 54 , and hsa-miR-23, which enhances oligodendrocyte differentiation and myelin synthesis 55”
From Human brain microRNAs exhibit cell-type specificity and age dependence (2026) · cites this paper as [54]
miR-375, miR-141, and miR-200a were enriched in the pituitary.
“miR-375, miR-141, and miR-200a in the pituitary (Landgraf et al. 2007);”
From MicroRNA expression in the adult mouse central nervous system (2008) · cites this paper as Landgraf et al. 2007
Some small ncRNAs are expressed in a tissue-, cell type-, or cell state-specific manner.
“with some being shown to be expressed in a tissue- (16), cell type- (17), or even cell state-specific manner (18)”
From A mouse tissue atlas of small noncoding RNA (2020) · cites this paper as [16]
Recent profiling of miRNA across cells and tissues demonstrated the existence of tissue- and cell type-specific short noncoding transcripts.
“Recent efforts in profiling of the most studied types of small ncRNA, miRNA, across cells and tissues demonstrated the existence of tissue- and cell type-specific short noncoding transcripts (16, 24, 25, 33).”
From A mouse tissue atlas of small noncoding RNA (2020) · cites this paper as [16]
Well-described brain-specific miRNAs include mir-9, mir-124, mir-219, mir-338, and miRNAs missing from existing catalogs include mir-666, mir-878, mir-433.
“We identified both well-described brain-specific miRNAs, such as mir-9, mir-124, mir-219, mir-338 (16, 24, 33), as well as those which are missing from existing catalogs, such as mir-666, mir-878, mir-433, etc.”
From A mouse tissue atlas of small noncoding RNA (2020) · cites this paper as [16]
A group of brain specific miRNAs, such as miR-124, miR-29b and miR-9, were highly enriched in all samples.
“Consistent with previous reports, we observed that a group of miRNAs known to be brain specific, such as miR-124, miR-29b and miR-9, were highly enriched in all the samples. (Bak et al., 2008, Landgraf et al., 2007).”
From Cell-Type-Based Analysis of MicroRNA Profiles in the Mouse Brain (2012) · cites this paper as Landgraf et al., 2007
The most thorough microRNA localization projects performed small RNA-seq on over 250 libraries from 26 organ systems but sequenced only approximately 1200 reads per library.
“The most thorough of these microRNA localization projects performed small RNA library sequencing (RNA-seq) on over 250 libraries from 26 organ systems. However, this nascent effort sequenced only ∼1200 reads per library (Landgraf et al. 2007).”
From Toward the human cellular microRNAome (2017) · cites this paper as Landgraf et al. 2007
miR-155 expression was highly specific to cells of hematopoietic origin.
“a previous study showed that miR-155 expression was highly specific to cells of hematopoietic origin 51 .”
From Identification of a protective microglial state mediated by miR-155 and interferon-γ signaling in a mouse model of Alzheimer’s disease (2023) · cites this paper as [51]
Landgraf et al. 2007 reported the first and most comprehensive analysis of miRNA abundance in different tissues.
“The first and as of now most comprehensive analysis of miRNA abundance in different tissues has been reported by Landgraf et al. in 2007 (3).”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
Landgraf et al. found high concordance of tissue-specific expression in humans and rodents for canonical miRNAs.
“For canonical miRNAs they found a high concordance of tissue-specific expression in humans and rodents.”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
Landgraf et al. 2007 reported 340 miRNAs in 26 organs.
“This sequencing-based study reported 340 miRNAs in 26 organs.”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
Landgraf et al. detected tissue-specific expression of miR-122 in liver, miR-9, miR-124 and miR-128a/b in brain, miR-7, miR-375, miR-141 and miR-200a in pituitary gland, and miR-142, miR-144, miR-150, miR-155 and miR-223 in hematopoietic cells.
“Amongst others, Landgraf et al. detected tissue-specific expression of miR-122 in liver, of miR-9, miR-124 and miR 128a/b in brain, of miR-7, miR-375, miR-141 and miR-200a in pituitary gland and of miR-142, miR-144, miR-150, miR-155 and miR-223 in hematopoietic cells.”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
The most comprehensive study on tissue-specific miRNAs in humans as of now was published by Landgraf et al. in 2007 (3).
“The, as of now, most comprehensive study on tissue-specific miRNAs in humans was published by Landgraf et al. in 2007 (3).”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
Landgraf et al. identified 340 mature human miRNAs including 33 novel miRNAs not listed in miRBase version 9.1.
“They identified 340 mature human miRNAs including 33 novel miRNAs not listed in the miRBase version 9.1, which was the current version at the time of the study (17).”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
Landgraf et al. identified miR-124 (miR-124-3p) as the third most specific miRNA in the nervous system.
“MiR-124 (miR-124–3p) was identified as the third most specific miRNA in the nervous system by Landgraf et al.”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
Landgraf et al. sequenced 256 small RNA libraries from 26 different organ systems and cell types of humans and rodents, with ∼1000 clones each.
“They sequenced 256 small RNA libraries from 26 different organ systems and cell types of humans and rodents, with ∼1000 clone each.”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
miR-514a-3p belongs to the miR-506 family; the mouse orthologue of miR-506, mmu-201, has been shown to be specifically expressed in reproductive tissues (3).
“MiR-514a-3p belongs to the miR-506 family; the mouse orthologue of miR-506, mmu-201, has been shown to be specifically expressed in reproductive tissues (3).”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
Loss-of-function of let-7, miR-124, miR-125 and miR-132 caused marked pruning of the dendritic arbor in hippocampal neurons.
“Loss-of-function of the abundant neuronal miRNAs let-7 and miR-124, and of the less abundant miR-125 and miR-132 (Landgraf et al., 2007), caused a marked pruning of the dendritic arbor, as quantified by Sholl analysis (Figure 4A, E).”
From Regulation of Synaptic Structure and Function by FMRP-Associated MicroRNAs miR-125b and miR-132 (2010) · cites this paper as Landgraf et al., 2007
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
Lewis, B. P., Burge, C. B., & Bartel, D. P. (2005) · Cell · doi:10.1016/j.cell.2004.12.035 · Cited by 11,855 · see citing works
Identification of Novel Genes Coding for Small Expressed RNAs
Lagos-Quintana, M., Rauhut, R., Lendeckel, W., & Tuschl, T. (2001) · Science · doi:10.1126/science.1064921 · Cited by 4,956 · see citing works
Self-citationMicroarray analysis shows that some microRNAs downregulate large numbers of target mRNAs
Lim, L. P., Lau, N. C., Garrett-Engele, P., Grimson, A., Schelter, J. M., Castle, J., Bartel, D. P., Linsley, P. S., & Johnson, J. M. (2005) · Nature · doi:10.1038/nature03315 · Cited by 4,755 · see citing works
miRBase: microRNA sequences, targets and gene nomenclature
Griffiths‐Jones, S. (2005) · Nucleic Acids Research · doi:10.1093/nar/gkj112 · Cited by 4,713 · see citing works
MicroRNA genes are transcribed by RNA polymerase II
Lee, Y., Kim, M., Han, J., Yeom, K.-H., Lee, S., Baek, S. H., & Kim, V. N. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600385 · Cited by 4,355 · see citing works
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 4,333 · see citing works
Wightman, B., Ha, I., & Ruvkun, G. (1993) · Cell · doi:10.1016/0092-8674(93)90530-4 · Cited by 4,292 · see citing works
Silencing of microRNAs in vivo with ‘antagomirs’
Krützfeldt, J., Rajewsky, N., Braich, R., Rajeev, K. G., Tuschl, T., Manoharan, M., & Stoffel, M. (2005) · Nature · doi:10.1038/nature04303 · Cited by 3,949 · see citing works
Self-citationHOW CELLS RESPOND TO INTERFERONS
Stark, G. R., Kerr, I. M., Williams, B. R. G., Silverman, R. H., & Schreiber, R. D. (1998) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.67.1.227 · Cited by 3,932 · see citing works
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 2,859 · see citing works
Self-citationAn Abundant Class of Tiny RNAs with Probable Regulatory Roles in <i>Caenorhabditis elegans</i>
Lau, N. C., Lim, L. P., Weinstein, E. G., & Bartel, D. P. (2001) · Science · doi:10.1126/science.1065062 · Cited by 2,713 · see citing works
Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA
Pasquinelli, A. E., Reinhart, B. J., Slack, F. J., Martindale, M. Q., Kuroda, M. I., Maller, B., Hayward, D. C., Ball, E. E., Degnan, B. M., Müller, P., et al. (2000) · Nature · doi:10.1038/35040556 · Cited by 2,568 · see citing works
MicroRNA-21 Is an Antiapoptotic Factor in Human Glioblastoma Cells
Chan, J. A., Krichevsky, A. M., & Kosik, K. S. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-0137 · Cited by 2,557 · see citing works
An Extensive Class of Small RNAs in <i>Caenorhabditis elegans</i>
Lee, R. C., & Ambros, V. (2001) · Science · doi:10.1126/science.1065329 · Cited by 2,358 · see citing works
A pancreatic islet-specific microRNA regulates insulin secretion
Poy, M. N., Eliasson, L., Krutzfeldt, J., Kuwajima, S., Ma, X., MacDonald, P. E., Pfeffer, S., Tuschl, T., Rajewsky, N., Rorsman, P., et al. (2004) · Nature · doi:10.1038/nature03076 · Cited by 2,102 · see citing works
Self-citationA uniform system for microRNA annotation
Ambros, V., Bartel, B., Bartel, D. P., Burge, C. B., Carrington, J. C., Chen, X., Dreyfuss, G., Eddy, S. R., Griffiths‐Jones, S., Marshall, M. S., et al. (2003) · RNA · doi:10.1261/rna.2183803 · Cited by 1,885 · see citing works
Self-citationXie, X., Lu, J., Kulbokas, E. J., Golub, T. R., Mootha, V., Lindblad-Toh, K., Lander, E. S., & Kellis, M. (2005) · Nature · doi:10.1038/nature03441 · Cited by 1,872 · see citing works
Current Protocols in Molecular Biology
Teplitz, R. L. (1989) · JAMA · doi:10.1001/jama.1989.03420090114049 · Cited by 1,848 · see citing works
MicroRNA Expression in Zebrafish Embryonic Development
Wienholds, E., Kloosterman, W. P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., de Bruijn, E., Horvitz, H. R., Kauppinen, S., & Plasterk, R. H. A. (2005) · Science · doi:10.1126/science.1114519 · Cited by 1,551 · see citing works
The Widespread Impact of Mammalian MicroRNAs on mRNA Repression and Evolution
Farh, K. K.-H., Grimson, A., Jan, C., Lewis, B. P., Johnston, W. K., Lim, L. P., Burge, C. B., & Bartel, D. P. (2005) · Science · doi:10.1126/science.1121158 · Cited by 1,484 · see citing works
Identification of hundreds of conserved and nonconserved human microRNAs
Bentwich, I., Avniel, A., Karov, Y., Aharonov, R., Gilad, S., Barad, O., Barzilai, A., Einat, P., Einav, U., Meiri, E., et al. (2005) · Nature Genetics · doi:10.1038/ng1590 · Cited by 1,465 · see citing works
BASKERVILLE, S., & BARTEL, D. P. (2005) · RNA · doi:10.1261/rna.7240905 · Cited by 1,241 · see citing works
Identification of microRNAs of the herpesvirus family
Pfeffer, S., Sewer, A., Lagos‐Quintana, M., Sheridan, R., Sander, C., Grässer, F. A., van Dyk, L. F., Ho, C. K., Shuman, S., Chien, M., et al. (2005) · Nature Methods · doi:10.1038/nmeth746 · Cited by 1,153 · see citing works
Self-citationmicroRNA target predictions in animals
Rajewsky, N. (2006) · Nature Genetics · doi:10.1038/ng1798 · Cited by 1,092 · see citing works
Stark, A., Brennecke, J., Bushati, N., Russell, R. B., & Cohen, S. M. (2005) · Cell · doi:10.1016/j.cell.2005.11.023 · Cited by 1,080 · see citing works
Kögler, G., Sensken, S., Airey, J. A., Trapp, T., Müschen, M., Feldhahn, N., Liedtke, S., Sorg, R. V., Fischer, J., Rosenbaum, C., et al. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20040440 · Cited by 1,029 · see citing works
Self-citationPhylogenetic Shadowing and Computational Identification of Human microRNA Genes
Berezikov, E., Guryev, V., van de Belt, J., Wienholds, E., Plasterk, R. H. A., & Cuppen, E. (2005) · Cell · doi:10.1016/j.cell.2004.12.031 · Cited by 1,008 · see citing works
Cummins, J. M., He, Y., Leary, R. J., Pagliarini, R. A., Diaz, L. A., Sjöblom, T., Barad, O., Bentwich, Z., Szafranska, A. E., Labourier, E., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511155103 · Cited by 927 · see citing works
Functions of microRNAs and related small RNAs in plants
Mallory, A. C., & Vaucheret, H. (2006) · Nature Genetics · doi:10.1038/ng1791 · Cited by 816 · see citing works
MicroRNA function in animal development
Wienholds, E., & Plasterk, R. H. A. (2005) · FEBS Letters · doi:10.1016/j.febslet.2005.07.070 · Cited by 811 · see citing works
Modulation of microRNA processing and expression through RNA editing by ADAR deaminases
Yang, W., Chendrimada, T. P., Wang, Q., Higuchi, M., Seeburg, P. H., Shiekhattar, R., & Nishikura, K. (2005) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1041 · Cited by 787 · see citing works
Redirection of Silencing Targets by Adenosine-to-Inosine Editing of miRNAs
Kawahara, Y., Zinshteyn, B., Sethupathy, P., Iizasa, H., Hatzigeorgiou, A. G., & Nishikura, K. (2007) · Science · doi:10.1126/science.1138050 · Cited by 785 · see citing works
Extensive post-transcriptional regulation of microRNAs and its implications for cancer
Thomson, J. M., Newman, M., Parker, J. S., Morin-Kensicki, E. M., Wright, T., & Hammond, S. M. (2006) · Genes & Development · doi:10.1101/gad.1444406 · Cited by 755 · see citing works
Moss, E. G., Lee, R. C., & Ambros, V. (1997) · Cell · doi:10.1016/s0092-8674(00)81906-6 · Cited by 723 · see citing works
New microRNAs from mouse and human
LAGOS-QUINTANA, M., RAUHUT, R., MEYER, J., BORKHARDT, A., & TUSCHL, T. (2003) · RNA · doi:10.1261/rna.2146903 · Cited by 714 · see citing works
Self-citationJin, P., Zarnescu, D. C., Ceman, S., Nakamoto, M., Mowrey, J., Jongens, T. A., Nelson, D. L., Moses, K., & Warren, S. T. (2004) · Nature Neuroscience · doi:10.1038/nn1174 · Cited by 604 · see citing works
Dynamics of Mammalian Chromosome Evolution Inferred from Multispecies Comparative Maps
Murphy, W. J., Larkin, D. M., der Wind, A. E.-V., Bourque, G., Tesler, G., Auvil, L. S., Beever, J. E., Chowdhary, B. P., Galibert, F., Gatzke, L., et al. (2005) · Science · doi:10.1126/science.1111387 · Cited by 594 · see citing works
Transcripts Targeted by the MicroRNA-16 Family Cooperatively Regulate Cell Cycle Progression
Linsley, P. S., Schelter, J., Burchard, J., Kibukawa, M., Martin, M. M., Bartz, S. R., Johnson, J. M., Cummins, J. M., Raymond, C. K., Dai, H., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02005-06 · Cited by 552 · see citing works
Cell-type-specific signatures of microRNAs on target mRNA expression
Sood, P., Krek, A., Zavolan, M., Macino, G., & Rajewsky, N. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511045103 · Cited by 547 · see citing works
Self-citationIn situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes
Kloosterman, W. P., Wienholds, E., de Bruijn, E., Kauppinen, S., & Plasterk, R. H. A. (2006) · Nature Methods · doi:10.1038/nmeth843 · Cited by 540 · see citing works
Widespread RNA Editing of EmbeddedAluElements in the Human TranscriptomePreprint
Kim, D. D. Y., Kim, T. T. Y., Walsh, T., Kobayashi, Y., Matise, T. C., Buyske, S. G., & Gabriel, A. (2004) · Genome Research · doi:10.1101/gr.2855504 · Cited by 534 · see citing works
Complex modulation of cell type-specific signaling in response to type I interferons
van Boxel-Dezaire, A. H. H., Rani, M. R. S., & Stark, G. R. (2006) · Immunity · doi:10.1016/j.immuni.2006.08.014 · Cited by 530 · see citing works
MicroRNAs: regulators of gene expression and cell differentiation
Shivdasani, R. A. (2006) · Blood · doi:10.1182/blood-2006-01-030015 · Cited by 501 · see citing works
Fragile X-related protein and VIG associate with the RNA interference machinery
Caudy, A. A., Myers, M., Hannon, G. J., & Hammond, S. M. (2002) · Genes & Development · doi:10.1101/gad.1025202 · Cited by 499 · see citing works
Micro RNAs in Animal Development
Plasterk, R. H. A. (2006) · Cell · doi:10.1016/j.cell.2006.02.030 · Cited by 437 · 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
Diversity of microRNAs in human and chimpanzee brain
Berezikov, E., Thuemmler, F., van Laake, L. W., Kondova, I., Bontrop, R., Cuppen, E., & Plasterk, R. H. A. (2006) · Nature Genetics · doi:10.1038/ng1914 · Cited by 416 · see citing works
Cullen, B. R. (2006) · Nature Genetics · doi:10.1038/ng1793 · Cited by 406 · see citing works
Post-transcriptional regulation of microRNA expression
Obernosterer, G., Leuschner, P. J. F., Alenius, M., & Martinez, J. (2006) · RNA · doi:10.1261/rna.2322506 · Cited by 391 · see citing works
RNA editing of human microRNAs
Blow, M. J., Grocock, R., van Dongen, S., Enright, A. J., Dicks, E., Futreal, P. A., Wooster, R., & Stratton, M. R. (2006) · Genome biology · doi:10.1186/gb-2006-7-4-r27 · Cited by 339 · see citing works
RNA editing of a miRNA precursor: FIGURE 1.
LUCIANO, D. J., Mirsky, H. P., Vendetti, N. J., & Maas, S. (2004) · RNA · doi:10.1261/rna.7350304 · Cited by 311 · see citing works
Mammalian microRNAs derived from genomic repeats
Smalheiser, N. R., & Torvik, V. I. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.04.008 · Cited by 293 · see citing works
Many novel mammalian microRNA candidates identified by extensive cloning and RAKE analysisPreprint
Berezikov, E., van Tetering, G., Verheul, M., van de Belt, J., Laake, L. W. V., Vos, J. B., Verloop, R. E., van de Wetering, M., Guryev, V., Takada, S., et al. (2006) · Genome Research · doi:10.1101/gr.5159906 · Cited by 273 · see citing works
Strategies to determine the biological function of microRNAs
Krützfeldt, J., Poy, M. N., & Stoffel, M. (2006) · Nature Genetics · doi:10.1038/ng1799 · Cited by 257 · see citing works
RAKE and LNA-ISH reveal microRNA expression and localization in archival human brain
NELSON, P. T., BALDWIN, D. A., KLOOSTERMAN, W. P., KAUPPINEN, S., PLASTERK, R. H. A., & MOURELATOS, Z. (2006) · RNA · doi:10.1261/rna.2258506 · Cited by 251 · see citing works
Identification and characterization of small RNAs involved in RNA silencing
Aravin, A. A., & Tuschl, T. (2005) · FEBS Letters · doi:10.1016/j.febslet.2005.08.009 · Cited by 240 · see citing works
Self-citationPolymorphisms in human pre-miRNAs
Iwai, N., & Naraba, H. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.04.051 · Cited by 202 · see citing works
Diederichs, S., & Haber, D. A. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0537 · Cited by 176 · see citing works
Cloning and expression of new microRNAs from zebrafish
Kloosterman, W. P., Steiner, F. A., Berezikov, E., de Bruijn, E., van de Belt, J., Verheul, M., Cuppen, E. P. J. G., & Plasterk, R. H. A. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl278 · Cited by 171 · see citing works
Gottwein, E., Cai, X., & Cullen, B. R. (2006) · Journal of Virology · doi:10.1128/jvi.02734-05 · Cited by 140 · see citing works
Is abundant A-to-I RNA editing primate-specific?
Eisenberg, E., Nemzer, S., Kinar, Y., Sorek, R., Rechavi, G., & Levanon, E. Y. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.12.005 · Cited by 128 · see citing works
Rigoutsos, I., Huynh, T., Miranda, K. C., Tsirigos, A., McHardy, A. C., & Platt, D. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601688103 · Cited by 127 · see citing works
Mouse microRNA profiles determined with a new and sensitive cloning method
Takada, S., Berezikov, E., Yamashita, Y., Lagos‐Quintana, M., Kloosterman, W. P., Enomoto, M., Hatanaka, H., Fujiwara, S., Watanabe, H., Soda, M., et al. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl653 · Cited by 102 · see citing works
The role of microRNAs in normal hematopoiesis and hematopoietic malignancies
Kluiver, J. L., Kroesen, B. J., Poppema, S., & van den Berg, A. (2006) · Leukemia · doi:10.1038/sj.leu.2404387 · Cited by 100 · see citing works
Camels and zebrafish, viruses and cancer: a microRNA update
Berezikov, E., & Plasterk, R. H. A. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi271 · Cited by 98 · see citing works
Cloning of Small RNA Molecules
Pfeffer, S., Lagos‐Quintana, M., & Tuschl, T. (2005) · Current Protocols in Molecular Biology · doi:10.1002/0471142727.mb2604s72 · Cited by 96 · see citing works
Self-citationDose-Dependent Inhibition of Thyroid Differentiation by RAS Oncogenes
Vita, G. D., Bauer, L., da Costa, V. M. C., Felice, M. D., Baratta, M. G., Menna, M. D., & Lauro, R. D. (2004) · Molecular Endocrinology · doi:10.1210/me.2004-0172 · Cited by 64 · see citing works
Plante, I., Davidovic, L., Ouellet, D. L., Gobeil, L.-A., Tremblay, S., Khandjian, E. W., & Provost, P. (2006) · BioMed Research International · doi:10.1155/jbb/2006/64347 · Cited by 52 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
MicroRNAs: Target Recognition and Regulatory Functions
Bartel, D. P. (2009) · Cell · doi:10.1016/j.cell.2009.01.002 · Cited by 20,068 · see citing works
Most mammalian mRNAs are conserved targets of microRNAs
Friedman, R. C., Farh, K. K.-H., Burge, C. B., & Bartel, D. P. (2009) · Genome Research · doi:10.1101/gr.082701.108 · Cited by 8,462 · see citing works
Circular RNAs are a large class of animal RNAs with regulatory potency
Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., Maier, L., Mackowiak, S. D., Gregersen, L. H., Munschauer, M., et al. (2013) · Nature · doi:10.1038/nature11928 · Cited by 7,990 · see citing works
Self-citationmiRBase: tools for microRNA genomics
Griffiths‐Jones, S., Saini, H. K., van Dongen, S., & Enright, A. J. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm952 · Cited by 4,349 · see citing works
MicroRNA Targeting Specificity in Mammals: Determinants beyond Seed Pairing
Grimson, A., Farh, K. K.-H., Johnston, W. K., Garrett-Engele, P., Lim, L. P., & Bartel, D. P. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.06.017 · Cited by 3,766 · see citing works
Bartel, D. P. (2018) · Cell · doi:10.1016/j.cell.2018.03.006 · Cited by 3,751 · see citing works
Widespread changes in protein synthesis induced by microRNAs
Selbach, M., Schwanhäusser, B., Thierfelder, N., Fang, Z., Khanin, R., & Rajewsky, N. (2008) · Nature · doi:10.1038/nature07228 · Cited by 3,429 · see citing works
Biogenesis of small RNAs in animals
Kim, V. N., Han, J., & Siomi, M. C. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2632 · Cited by 3,181 · see citing works
Transcriptome-wide Identification of RNA-Binding Protein and MicroRNA Target Sites by PAR-CLIP
Hafner, M., Landthaler, M., Burger, L., Khorshid, M., Hausser, J., Berninger, P., Rothballer, A., Ascano, M., Jungkamp, A.-C., Munschauer, M., et al. (2010) · Cell · doi:10.1016/j.cell.2010.03.009 · Cited by 2,873 · see citing works
Self-citationThe microRNA.org resource: targets and expression
Betel, D., Wilson, M. T., Gabow, A. P., Marks, D. S., & Sander, C. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm995 · Cited by 2,490 · see citing works
Self-citationSmall silencing RNAs: an expanding universe
Ghildiyal, M., & Zamore, P. D. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2504 · Cited by 2,314 · see citing works
Gao, P., Tchernyshyov, I., Chang, T.-C., Lee, Y.-S., Kita, K., Ochi, T., Zeller, K. I., De Marzo, A. M., Van Eyk, J. E., Mendell, J. T., et al. (2009) · Nature · doi:10.1038/nature07823 · Cited by 2,124 · see citing works
Regulation of microRNA function in animals
Gebert, L. F. R., & MacRae, I. J. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0045-7 · Cited by 2,031 · see citing works
miRTarBase 2016: updates to the experimentally validated miRNA-target interactions database
Chou, C., Chang, N.-W., Shrestha, S., Hsu, S., Lin, Y., Lee, W.-H., Yang, C.-D., Hong, H.-C., Wei, T., Tu, S.-J., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1258 · Cited by 1,829 · see citing works
The Endothelial-Specific MicroRNA miR-126 Governs Vascular Integrity and Angiogenesis
Wang, S., Aurora, A. B., Johnson, B. A., Qi, X., McAnally, J., Hill, J. A., Richardson, J. A., Bassel‐Duby, R., & Olson, E. N. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.07.002 · Cited by 1,825 · see citing works
Argonaute HITS-CLIP decodes microRNA–mRNA interaction maps
Chi, S. W., Zang, J. B., Mele, A., & Darnell, R. B. (2009) · Nature · doi:10.1038/nature08170 · Cited by 1,791 · see citing works
Therapeutic microRNA Delivery Suppresses Tumorigenesis in a Murine Liver Cancer Model
Kota, J., Chivukula, R. R., O’Donnell, K. A., Wentzel, E. A., Montgomery, C. L., Hwang, H., Chang, T.-C., Vivekanandan, P., Torbenson, M. S., Clark, K. R., et al. (2009) · Cell · doi:10.1016/j.cell.2009.04.021 · Cited by 1,711 · see citing works
MicroRNAs in Stress Signaling and Human Disease
Mendell, J. T., & Olson, E. N. (2012) · Cell · doi:10.1016/j.cell.2012.02.005 · Cited by 1,673 · see citing works
Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites
Betel, D., Koppal, A., Agius, P., Sander, C., & Leslie, C. (2010) · Genome Biology · doi:10.1186/gb-2010-11-8-r90 · Cited by 1,592 · see citing works
Self-citationThe biochemical basis of microRNA targeting efficacy
(2019) · doi:10.1126/science.aav1741 · Cited by 1,570 · see citing works
The evolution of gene regulation by transcription factors and microRNAs
Chen, K., & Rajewsky, N. (2007) · Nature Reviews Genetics · doi:10.1038/nrg1990 · Cited by 1,547 · see citing works
MicroRNA-10a binds the 5’UTR of ribosomal protein mRNAs and enhances their translation
Ørom, U. A., Nielsen, F. C., & Lund, A. H. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.05.001 · Cited by 1,384 · see citing works
Small non-coding RNAs in animal development
Stefani, G., & Slack, F. J. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2347 · Cited by 1,361 · see citing works
Connecting microRNA Genes to the Core Transcriptional Regulatory Circuitry of Embryonic Stem Cells
Marson, A., Levine, S. S., Cole, M. F., Frampton, G. M., Brambrink, T., Johnstone, S. E., Guenther, M. G., Johnston, W. K., Wernig, M., Newman, J. J., et al. (2008) · Cell · doi:10.1016/j.cell.2008.07.020 · Cited by 1,361 · see citing works
Distinctive chromatin in human sperm packages genes for embryo development
Hammoud, S. S., Nix, D. A., Zhang, H., Purwar, J., Carrell, D. T., & Cairns, B. R. (2009) · Nature · doi:10.1038/nature08162 · Cited by 1,326 · see citing works
Genetic variation in microRNA networks: the implications for cancer research
Ryan, B. M., Robles, A. I., & Harris, C. C. (2010) · Nature reviews. Cancer · doi:10.1038/nrc2867 · Cited by 1,253 · see citing works
Discovering microRNAs from deep sequencing data using miRDeep
Friedländer, M. R., Chen, W., Adamidi, C., Maaskola, J., Einspanier, R., Knespel, S., & Rajewsky, N. (2008) · Nature Biotechnology · doi:10.1038/nbt1394 · Cited by 1,189 · see citing works
Diversifying microRNA sequence and function
Ameres, S. L., & Zamore, P. D. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3611 · Cited by 1,175 · see citing works
Wang, G., Zhu, J., Zhang, J., Li, Q., Li, Y., He, J., Qin, Y., & Jing, Q. (2010) · European Heart Journal · doi:10.1093/eurheartj/ehq013 · Cited by 1,168 · see citing works
DIANA-microT web server v5.0: service integration into miRNA functional analysis workflows
Paraskevopoulou, M. D., Georgakilas, G. K., Kostoulas, N., Vlachos, I. S., Vergoulis, T., Reczko, M., Filippidis, C., Dalamagas, T., & Hatzigeorgiou, A. G. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt393 · Cited by 1,132 · see citing works
MicroRNA-145 Regulates OCT4, SOX2, and KLF4 and Represses Pluripotency in Human Embryonic Stem Cells
Xu, N., Papagiannakopoulos, T. Y., Pan, G., Thomson, J. A., & Kosik, K. S. (2009) · Cell · doi:10.1016/j.cell.2009.02.038 · Cited by 1,128 · see citing works
MicroRNAs: new regulators of immune cell development and function
Baltimore, D., Boldin, M., O’Connell, R. M., Rao, D. S., & Taganov, K. D. (2008) · Nature Immunology · doi:10.1038/ni.f.209 · Cited by 1,083 · see citing works
Mohr, A. M., & Mott, J. L. (2015) · Seminars in Liver Disease · doi:10.1055/s-0034-1397344 · Cited by 1,076 · see citing works
Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes
Tam, O. H., Aravin, A. A., Stein, P., Girard, A., Murchison, E. P., Cheloufi, S., Hodges, E. C., Anger, M., Sachidanandam, R., Schultz, R. M., et al. (2008) · Nature · doi:10.1038/nature06904 · Cited by 1,042 · see citing works
Self-citationMicroRNA Control in the Immune System: Basic Principles
Xiao, C., & Rajewsky, K. (2009) · Cell · doi:10.1016/j.cell.2008.12.027 · Cited by 1,008 · see citing works
MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1
Harris-Tryon, T. A., Yamakuchi, M., Ferlito, M., Mendell, J. T., & Lowenstein, C. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707493105 · Cited by 1,007 · see citing works
miR‐21: a small multi‐faceted RNA
Krichevsky, A. M., & Gabriely, G. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2008.00556.x · Cited by 987 · see citing works
Morin, R. D., O’Connor, M. D., Griffith, M., Kuchenbauer, F., Delaney, A., Prabhu, A.-L., Zhao, Y., McDonald, H., Zeng, T., Hirst, M., et al. (2008) · Genome Research · doi:10.1101/gr.7179508 · Cited by 972 · see citing works
MicroRNAs accurately identify cancer tissue origin
Rosenfeld, N., Aharonov, R., Meiri, E., Rosenwald, S., Spector, Y., Zepeniuk, M., Benjamin, H., Shabes, N., Tabak, S., Levy, A., et al. (2008) · Nature Biotechnology · doi:10.1038/nbt1392 · Cited by 971 · see citing works
Distribution of miRNA expression across human tissues
Ludwig, N., Leidinger, P., Becker, K., Backes, C., Fehlmann, T., Pallasch, C., Rheinheimer, S., Meder, B., Stähler, C., Meese, E., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw116 · Cited by 968 · see citing works
A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance
van Rooij, E., Quiat, D., Johnson, B. A., Sutherland, L. B., Qi, X., Richardson, J. A., Kelm, R. J., & Olson, E. N. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.10.013 · Cited by 960 · see citing works
Lin28 Mediates the Terminal Uridylation of let-7 Precursor MicroRNA
Heo, I., Joo, C., Cho, J., Ha, M., Han, J., & Kim, V. N. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.09.014 · Cited by 947 · see citing works
MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy
Kasinski, A. L., & Slack, F. J. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3166 · Cited by 934 · see citing works
An Analysis of Human MicroRNA and Disease Associations
Lü, M., Zhang, Q., Deng, M., Miao, J., Guo, Y., Gao, W., & Cui, Q. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003420 · Cited by 899 · see citing works
Farazi, T. A., Spitzer, J., Morozov, P. S., & Tuschl, T. (2010) · The Journal of Pathology · doi:10.1002/path.2806 · Cited by 892 · see citing works
Self-citationMicroRNA 21 Promotes Glioma Invasion by Targeting Matrix Metalloproteinase Regulators
Gabriely, G., Wurdinger, T., Kesari, S., Esau, C. C., Burchard, J., Linsley, P. S., & Krichevsky, A. M. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00479-08 · Cited by 888 · see citing works
<i>miR-146a</i> is a significant brake on autoimmunity, myeloproliferation, and cancer in mice
Boldin, M. P., Taganov, K. D., Rao, D. S., Yang, L., Zhao, J. L., Kalwani, M., Garcia-Flores, Y., Luong, M., Devrekanli, A., Xu, J., et al. (2011) · Journal of Experimental Medicine · doi:10.1084/jem.20101823 · Cited by 861 · see citing works
Garcia, D. M., Baek, D., Shin, C., Bell, G. W., Grimson, A., & Bartel, D. P. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2115 · Cited by 859 · see citing works
Exosomal cell-to-cell transmission of alpha synuclein oligomers
Danzer, K. M., Kranich, L. R., Ruf, W. P., Cagsal‐Getkin, O., Winslow, A. R., Zhu, L., Vanderburg, C. R., & McLean, P. J. (2012) · Molecular Neurodegeneration · doi:10.1186/1750-1326-7-42 · Cited by 852 · see citing works
MicroRNAs: the fine-tuners of Toll-like receptor signalling
O'Neill, L. A. J., Sheedy, F. J., & McCoy, C. E. (2011) · Nature reviews. Immunology · doi:10.1038/nri2957 · Cited by 851 · see citing works
Berezikov, E., Chung, W., Willis, J., Cuppen, E. P. J. G., & Lai, E. C. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.09.028 · Cited by 795 · see citing works
Ponomarev, 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
Paul, S., & Candelario‐Jalil, E. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113518 · Cited by 762 · see citing works
Khan, M., Nickoloff, E., Abramova, T. V., Johnson, J. A., Verma, S. K., Krishnamurthy, P., Mackie, A. R., Vaughan, E. E., Garikipati, V. N. S., Benedict, C., et al. (2015) · Circulation Research · doi:10.1161/circresaha.117.305990 · Cited by 754 · see citing works
Biomarkers of Acute Kidney Injury
Vaidya, V. S., Ferguson, M. A., & Bonventre, J. V. (2007) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.48.113006.094615 · Cited by 741 · see citing works
Wang, X., Tang, S., Le, S., Lu, R., Rader, J. S., Meyers, C., & Zheng, Z. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002557 · Cited by 736 · see citing works
Regulation of Synaptic Structure and Function by FMRP-Associated MicroRNAs miR-125b and miR-132
Edbauer, D., Neilson, J. R., Foster, K. A., Wang, C.-F., Seeburg, D. P., Batterton, M. N., Tada, T., Dolan, B. M., Sharp, P. A., & Sheng, M. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.005 · Cited by 735 · see citing works
Mammalian microRNAs: experimental evaluation of novel and previously annotated genes
Chiang, H. R., Schoenfeld, L. W., Ruby, J. G., Auyeung, V. C., Spies, N., Baek, D., Johnston, W. K., Russ, C., Luo, S., Babiarz, J. E., et al. (2010) · Genes & Development · doi:10.1101/gad.1884710 · Cited by 732 · see citing works
Multi-Input RNAi-Based Logic Circuit for Identification of Specific Cancer Cells
Xie, Z., Wróblewska, L., Prochazka, L., Weiss, R., & Benenson, Y. (2011) · Science · doi:10.1126/science.1205527 · Cited by 732 · see citing works
The biphasic function of microglia in ischemic stroke
Ma, Y., Wang, J., Wang, Y., & Yang, G. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.01.005 · Cited by 724 · see citing works
Assessing the ceRNA Hypothesis with Quantitative Measurements of miRNA and Target Abundance
Denzler, R., Agarwal, V., Stefano, J., Bartel, D. P., & Stoffel, M. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.03.045 · Cited by 723 · see citing works
Transcriptome-wide Analysis of Regulatory Interactions of the RNA-Binding Protein HuR
Lebedeva, S., Jens, M., Theil, K., Schwanhäusser, B., Selbach, M., Landthaler, M., & Rajewsky, N. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.06.008 · Cited by 716 · see citing works
Self-citationCeppi, M., Pereira, P. M., Dunand-Sauthier, I., Barras, E., Reith, W., Santos, M. A. S., & Pierre, P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811073106 · Cited by 713 · see citing works
Evolution of microRNA diversity and regulation in animals
Berezikov, E. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3079 · Cited by 712 · see citing works
Farazi, T. A., Hoell, J. I., Morozov, P. S., & Tuschl, T. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-5590-1_1 · Cited by 699 · see citing works
Self-citationOpposing microRNA families regulate self-renewal in mouse embryonic stem cells
Melton, C. A., Judson, R. L., & Blelloch, R. H. (2010) · Nature · doi:10.1038/nature08725 · Cited by 693 · see citing works
Hou, J., Lin, L., Zhou, W., Wang, Z., Ding, G., Dong, Q., Qin, L., Wu, X., Zheng, Y., Yang, Y. S., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.01.001 · Cited by 690 · see citing works
On the road to reading the RNA-interference code
Siomi, H., & Siomi, M. C. (2009) · Nature · doi:10.1038/nature07754 · Cited by 674 · see citing works
Chromatin structure analyses identify miRNA promotersPreprint
Ozsolak, F., Poling, L. L., Wang, Z., Liu, H., Liu, X., Roeder, R. G., Zhang, X., Song, J. S., & Fisher, D. E. (2008) · Genes & Development · doi:10.1101/gad.1706508 · Cited by 670 · see citing works
Ma, F., Xu, S., Liu, X., Zhang, Q., Xu, X., Liu, M., Hua, M.-M., Li, N., Yao, H., & Cao, X. (2011) · Nature Immunology · doi:10.1038/ni.2073 · Cited by 647 · see citing works
Boettger, T., Beetz, N., Sawa Kostin, D., Schneider, J., Krüger, M., Hein, L., & Braun, T. W. (2009) · Journal of Clinical Investigation · doi:10.1172/jci38864 · Cited by 644 · see citing works
Orang, A., Safaralizadeh, R., & Kazemzadeh, M. (2014) · International Journal of Genomics · doi:10.1155/2014/970607 · Cited by 644 · see citing works
miR-122 – A key factor and therapeutic target in liver disease
Bandiera, S., Pfeffer, S., Baumert, T. F., & Zeisel, M. B. (2014) · Journal of Hepatology · doi:10.1016/j.jhep.2014.10.004 · Cited by 633 · see citing works
Self-citationNon-coding RNAs as regulators of embryogenesis
Pauli, A., Rinn, J. L., & Schier, A. F. (2011) · Nature Reviews Genetics · doi:10.1038/nrg2904 · Cited by 623 · see citing works
Identification and consequences of miRNA–target interactions — beyond repression of gene expression
Hausser, J., & Zavolan, M. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3765 · Cited by 620 · see citing works
Self-citationMicroRNA regulation by RNA-binding proteins and its implications for cancer
van Kouwenhove, M., Kedde, M., & Agami, R. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3107 · Cited by 617 · see citing works
Git, A., Dvinge, H., Salmon-Divon, M., Osborne, M., Kutter, C., Hadfield, J., Bertone, P., & Caldas, C. (2010) · RNA · doi:10.1261/rna.1947110 · Cited by 607 · see citing works
let-7 microRNAs in development, stem cells and cancer
Büssing, I., Slack, F. J., & Großhans, H. (2008) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2008.07.001 · Cited by 604 · see citing works
Therapeutic Inhibition of miR-208a Improves Cardiac Function and Survival During Heart Failure
Montgomery, R. L., Hullinger, T. G., Semus, H. M., Dickinson, B., Seto, A. G., Lynch, J. M., Stack, C., Latimer, P. A., Olson, E. N., & van Rooij, E. (2011) · Circulation · doi:10.1161/circulationaha.111.030932 · Cited by 600 · see citing works
Dicer Ablation Affects Antibody Diversity and Cell Survival in the B Lymphocyte Lineage
Koralov, S. B., Muljo, S. A., Galler, G. R., Krek, A., Chakraborty, T., Kanellopoulou, C., Jensen, K., Cobb, B. S., Merkenschlager, M., Rajewsky, N., et al. (2008) · Cell · doi:10.1016/j.cell.2008.02.020 · Cited by 575 · see citing works
Posttranscriptional Regulation of MicroRNA Biogenesis in Animals
Siomi, H., & Siomi, M. C. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.03.013 · Cited by 574 · see citing works
TGF-β activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN
Kato, M. V., Putta, S., Wang, M., Yuan, H., Lanting, L. L., Nair, I., Gunn, A., Nakagawa, Y., Shimano, H., Todorov, I., et al. (2009) · Nature Cell Biology · doi:10.1038/ncb1897 · Cited by 572 · see citing works
MicroRNA-21 Is Up-Regulated in Allergic Airway Inflammation and Regulates IL-12p35 Expression
Lu, T. X., Munitz, A., & Rothenberg, M. E. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803560 · Cited by 569 · see citing works
A Role for Neuronal piRNAs in the Epigenetic Control of Memory-Related Synaptic Plasticity
Rajasethupathy, P., Antonov, I., Sheridan, R., Frey, S., Sander, C., Tuschl, T., & Kandel, E. R. (2012) · Cell · doi:10.1016/j.cell.2012.02.057 · Cited by 566 · see citing works
Self-citationChen, Z., Venkat, P., Seyfried, D., Chopp, M., Yan, T., & Chen, J. (2017) · Circulation Research · doi:10.1161/circresaha.117.311170 · Cited by 565 · see citing works
An integrated expression atlas of miRNAs and their promoters in human and mouse
The FANTOM Consortium, de Rie, D., Abugessaisa, I., Alam, T., Arner, E., Arner, P., Ashoor, H., Åström, G., Babina, M., Bertin, N., et al. (2017) · Nature Biotechnology · doi:10.1038/nbt.3947 · Cited by 561 · see citing works
MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression
Ivanovska, I., Ball, A. S., Diaz, R. L., Magnus, J. F., Kibukawa, M., Schelter, J. M., Kobayashi, S. V., Lim, L., Burchard, J., Jackson, A. L., et al. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01977-07 · Cited by 561 · see citing works
Brown, B. D., Gentner, B., Cantore, A., Colleoni, S., Amendola, M., Zingale, A., Baccarini, A., Lazzari, G., Galli, C., & Naldini, L. (2007) · Nature Biotechnology · doi:10.1038/nbt1372 · Cited by 559 · see citing works
Post-transcriptional control of miRNA biogenesis
Michlewski, G., & Cáceres, J. F. (2018) · RNA · doi:10.1261/rna.068692.118 · Cited by 559 · see citing works
The Role of MicroRNAs in Human Diseases.
Ardekani, A. M., & Naeini, M. M. (2010) · Europe PMC (PubMed Central) · Cited by 552 · see citing works
Elia, L., Quintavalle, M., Zhang, J., Contu, R., Cossu, L., Latronico, M. V. G., Peterson, K. L., Indolfi, C., Catalucci, D., Chen, J., et al. (2009) · Cell Death and Differentiation · doi:10.1038/cdd.2009.153 · Cited by 551 · see citing works
Segura, M. F., Hanniford, D., Menéndez, S., Reavie, L. B., Zou, X., Álvarez-Díaz, S., Zakrzewski, J., Blochin, E., Rose, A. E., Bogunovic, D., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808263106 · Cited by 538 · see citing works
MicroRNA‐29, a key regulator of collagen expression in systemic sclerosis
Maurer, B., Stańczyk, J., Jüngel, A., Akhmetshina, A., Trenkmann, M., Brock, M., Kowal‐Bielecka, O., Gay, R. E., Michel, B. A., Distler, J. H. W., et al. (2010) · Arthritis & Rheumatism · doi:10.1002/art.27443 · Cited by 536 · see citing works
van Rooij, E. (2011) · Circulation Research · doi:10.1161/circresaha.110.227496 · Cited by 534 · see citing works
Transfection of small RNAs globally perturbs gene regulation by endogenous microRNAs
Khan, A. A., Betel, D., Miller, M. L., Sander, C., Leslie, C. S., & Marks, D. S. (2009) · Nature Biotechnology · doi:10.1038/nbt.1543 · Cited by 534 · see citing works
Self-citationmicroRNAs and the immune response
Lindsay, M. A. (2008) · Trends in Immunology · doi:10.1016/j.it.2008.04.004 · Cited by 532 · see citing works
Coding and noncoding landscape of extracellular RNA released by human glioma stem cells
Wei, Z., Batagov, A. O., Schinelli, S., Wang, J., Wang, Y., Fatimy, R. E., Rabinovsky, R., Balaj, L., Chen, C. C., Hochberg, F. H., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01196-x · Cited by 532 · see citing works
Dicer1 and miR-219 Are Required for Normal Oligodendrocyte Differentiation and Myelination
Dugas, J. C., Cuellar, T. L., Scholze, A., Ason, B., Ibrahim, A., Emery, B., Zamanian, J. L., Foo, L. C., McManus, M. T., & Barres, B. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.027 · Cited by 527 · see citing works
Metazoan promoters: emerging characteristics and insights into transcriptional regulation
Lenhard, B., Sandelin, A., & Carninci, P. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3163 · Cited by 513 · see citing works
MicroRNAs as regulators of epithelial-mesenchymal transition
Gregory, P. A., Bracken, C. P., Bert, A. G., & Goodall, G. J. (2008) · Cell Cycle · doi:10.4161/cc.7.20.6851 · Cited by 506 · see citing works
- Authors
- Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., Pfeffer, S., Rice, A., Kamphorst, A. O., Landthaler, M., Lin, C., Socci, N. D., Hermida, L., Fulci, V., Chiaretti, S., Foà, R., Schliwka, J., Fuchs, U., Novosel, A., Müller, R.-U., Schermer, B., Bissels, U., Inman, J., Phan, Q., Chien, M., Weir, D. B., Choksi, R., De Vita, G., Frezzetti, D., Trompeter, H.-I., Hornung, V., Teng, G., Hartmann, G., Palkovits, M., Di Lauro, R., Wernet, P., Macino, G., Rogler, C. E., Nagle, J. W., Ju, J., Papavasiliou, F. N., Benzing, T., Lichter, P., Tam, W., Brownstein, M. J., Bosio, A., Borkhardt, A., Russo, J. J., Sander, C., Zavolan, M., & Tuschl, T.
- Affiliations
- Howard Hughes Medical Institute (US)
- University of Basel (CH)
- Memorial Sloan Kettering Cancer Center (US)
- SIB Swiss Institute of Bioinformatics (CH)
- Sapienza University of Rome (IT)
- German Cancer Research Center (DE)
- Ludwig-Maximilians-Universität München (DE)
- University Medical Center Freiburg (DE)
- Miltenyi Biotec (Germany) (DE)
- J. Craig Venter Institute (US)
- Columbia University (US)
- University of Naples Federico II (IT)
- Düsseldorf University Hospital (DE)
- Rockefeller University (US)
- University of Bonn (DE)
- Albert Einstein College of Medicine (US)
- National Institutes of Health (US)
- Cornell University (US)
- Corresponding author
- Zavolan, Mihaela
- Tuschl, Thomas
- ORCID
- Landgraf, Pablo
- Rusu, Mirabela
- Iovino, Nicola
- Aravin, Alexei
- Pfeffer, Sébastien
- Kamphorst, Alice O.
- Landthaler, Markus
- Lin, Carolina
- Socci, Nicholas D.
- Hermida, Leandro
- Fulci, Valerio
- Chiaretti, Sabina
- Foà, Robin
- Müller, Roman-Ulrich
- Schermer, Bernhard
- Inman, Jason
- Frezzetti, Daniela
- Trompeter, Hans-Ingo
- Hornung, Veit
- Hartmann, Gunther
- Papavasiliou, F. Nina
- Benzing, Thomas
- Tam, Wayne
- Bosio, Andreas
- Borkhardt, Arndt
- Russo, James J.
- Sander, Chris
- Zavolan, Mihaela
- Tuschl, Thomas
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2007-06
- Volume
- 129
- Issue
- 7
- Pages
- 1401-1414
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC2681231
- OpenAlex
- W2149146453
- Cited by
- 3,626
- References
- 70
- Citations by year
- 2026: 42 · 2025: 73 · 2024: 87 · 2023: 104 · 2022: 131 · 2021: 160 · 2020: 152 · 2019: 167 · 2018: 205 · 2017: 185 · 2016: 221 · 2015: 238 · 2014: 275 · 2013: 310 · 2012: 283
- FWCI
- 84.13
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2274 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- HAL (submittedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (105945, 205321)
- National Institute of General Medical Sciences (P01GM073047)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- microRNA, small RNA sequencing, microRNA precursors, microRNA maturation, miRNA conservation, microRNA target regulation, hematopoietic cells, neurons, cell lineage, miRNA expression profiling
- MeSH terms
- Animals, Base Sequence, Gene Expression Regulation, Hematopoietic Stem Cells, Humans, Molecular Sequence Data, Phylogeny, RNA, Messenger, Sequence Homology, Nucleic Acid, Gene Library, Conserved Sequence, Cell Lineage, Hematologic Neoplasms, Gene Expression Profiling, MicroRNAs, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
