The DOI matches its Crossref record; 106 of the 111 references it cites were found in a registry or an index.
Most Caenorhabditis elegans microRNAs Are Individually Not Essential for Development or Viability
Open accessAbstract
MicroRNAs (miRNAs), a large class of short noncoding RNAs found in many plants and animals, often act to post-transcriptionally inhibit gene expression. We report the generation of deletion mutations in 87 miRNA genes in Caenorhabditis elegans, expanding the number of mutated miRNA genes to 95, or 83% of known C. elegans miRNAs. We find that the majority of miRNAs are not essential for the viability or development of C. elegans, and mutations in most miRNA genes do not result in grossly abnormal phenotypes. These observations are consistent with the hypothesis that there is significant functional redundancy among miRNAs or among gene pathways regulated by miRNAs. This study represents the first comprehensive genetic analysis of miRNA function in any organism and provides a unique, permanent resource for the systematic study of miRNAs.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“which may help to explain the robustness of miRNA regulatory networks and their resilience to mutations of individual miRNAs in knockout experiments (Miska et al., 2007).”
From Scalable and deep profiling of mRNA targets for individual microRNAs with chimeric eCLIP (2022) · cites this paper as Miska et al., 2007
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Bartel (2004) · doi:10.1016/s0092-8674(04)00045-5 · Cited by 34,714
THE GENETICS OF CAENORHABDITIS ELEGANS
Brenner, S. (1974) · Genetics · doi:10.1093/genetics/77.1.71 · Cited by 15,161
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 · cited 2×
“We performed a broad phenotypic study of all available miRNA loss-of-function mutants, including mutants that had been reported earlier [2,4,20,52].”
BackgroundMethodSelf-citationLewis, B. P., Burge, C. B., & Bartel, D. P. (2005) · Cell · doi:10.1016/j.cell.2004.12.035 · Cited by 11,855 · cited 1×
“]. Because many messages have been under selective pressure to preserve pairing to a 6mer in the 5′ region of the miRNA known as the miRNA seed (nucleotides 2–7), targets of metazoan miRNAs can be predicted above the background of false-positives by searching for conserved matches to the seed region [”
BackgroundSelf-citationThe nuclear RNase III Drosha initiates microRNA processing
Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Rådmark, O., Kim, S., et al. (2003) · Nature · doi:10.1038/nature01957 · Cited by 5,294 · cited 1×
“In animals, miRNAs are transcribed as long RNA precursors (pri-miRNAs), which are processed in the nucleus by the RNase III enzyme complex Drosha-Pasha/DGCR8 to form the approximately 70-base pre-miRNAs [21–25] or are derived directly from introns [26,27].”
BackgroundPrediction 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 · cited 1×
“Because many messages have been under selective pressure to preserve pairing to a 6mer in the 59 region of the miRNA known as the miRNA seed (nucleotides 2–7), targets of metazoan miRNAs can be predicted above the background of false-positives by searching for conserved matches to the seed region [41–45].”
BackgroundSelf-citationThe 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
Self-citationIdentification 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 · cited 1×
“miRNAs have been identified in organisms as diverse as roundworms, flies, fish, frogs, mammals, flowering plants, mosses, and even viruses, using genetics, molecular cloning, and predictions from bioinformatics [7–16].”
BackgroundMicroarray 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
Self-citationSelf-assembly of mesoscopically ordered chromatic polydiacetylene/silica nanocomposites
Lu, Y.-F., Yang, Y., Sellinger, A., Lu, M.-C., Huang, J.-M., Fan, H., Haddad, R., López, G. P., Burns, A. R., Sasaki, D., et al. (2001) · Nature · doi:10.1038/35073544 · Cited by 4,708 · cited 2×
“We performed a broad phenotypic study of all available miRNA loss-of-function mutants, including mutants that had been reported earlier [2,4,20,52].”
BackgroundMethod
Research works printed but not linked: 3
- RubyJGStarkAJohnstonWKellisMBartelDP 2007 Biogenesis, expression, and target predictions for an expanded set of microRNA genes in Drosophila. Genome Res In press. · DOI
- WoodWB and the Community of C. elegans Researchers 1988 The nematode Caenorhabditis elegans Cold Spring Harbor, New York Cold Spring Harbor Press
- FixsenWD 1985 The genetic control of hypodermal cell lineages during nematode development [Ph.D.]. Cambridge Massachusetts Institute of Technology
Cited by
Sorted by citations
Items 301–400 of 454
Duan, H., de Navas, L. D., Hu, F., Sun, K.-L., Mavromatakis, Y., Viets, K., Zhou, C., Kavaler, J., Johnston, R., Tomlinson, A., et al. (2018) · Development · doi:10.1242/dev.159053 · Cited by 13
“On the other hand, systematic collections of miRNA deletions demonstrate that the vast majority do not cause seemingly overt phenotypes (Chen et al., 2014; Miska et al., 2007).”
BackgroundDeletion of Dicer in late erythroid cells results in impaired stress erythropoiesis in mice
Byon, J. C. H., Padilla, S. M., & Papayannopoulou, T. (2014) · Experimental Hematology · doi:10.1016/j.exphem.2014.06.004 · Cited by 12
“elegans, where the majority of single miRNA-deletion mutants did not have an appreciable phenotype [19].”
BackgroundThe Non-coding Road Towards Cardiac Regeneration
Hudson, J. E., & Porrello, E. R. (2013) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-013-9486-8 · Cited by 14
“It is thought that there may be considerable redundancy in miRNA activity as over 80 % of miRNAs have been deleted in Caenorhabditis elegans, with severe developmental defects only observed in less than 10 % of mutants [109].”
BackgroundManzano-Román, R., Oleaga, A., Pérez–Sánchez, R., & Siles‐Lucas, M. (2012) · Advances in Parasitology/Advances in parasitology · doi:10.1016/b978-0-12-394303-3.00002-5 · Cited by 14
miRNA-27a is essential for bone remodeling by modulating p62-mediated osteoclast signaling
Wang, S., Maruyama, E. O., Martinez, J. C., Lopes, J., Hsu, T., Wu, W., Hsu, W., & Maruyama, T. (2023) · eLife · doi:10.7554/elife.79768 · Cited by 12
“However, possibly due to functional redundancy, most of the miRNA deletions do not cause phenotypic alterations ( Miska et al., 2007 ; Park et al., 2012 ).”
An updated C. elegans nuclear body muscle transcriptome for studies in muscle formation and function
Schorr, A. L., Mejia, A. F., Miranda, M. Y., & Mangone, M. (2023) · bioRxiv · doi:10.1186/s13395-023-00314-2 · Cited by 12
Chang, S.-H., Su, Y., Chang, M., & Chen, J. (2021) · eLife · doi:10.7554/elife.63768 · Cited by 15
Dzakah, E. E., Waqas, A., Wei, S., Yu, B., Wang, X., Fu, T., Liu, L., & Shan, G. (2018) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2018.11.003 · Cited by 18
Cis-acting elements in its 3′ UTR mediate post-transcriptional regulation ofKRAS
Kim, M., Kogan, N., & Slack, F. J. (2016) · Oncotarget · doi:10.18632/oncotarget.7599 · Cited by 12
“This is not unexpected, since knocking down an individual miRNA often does not result in phenotypic changes [38], and a combination of miRNAs may cooperate for the full reporter repression.”
BackgroundGene targets of mouse miR-709: regulation of distinct pools
Surendran, S., Jideonwo, V., Merchun, C., Ahn, M., Murray, J. H., Ryan, J. C., Dunn, K., Kota, J., & Morral, N. (2016) · Scientific Reports · doi:10.1038/srep18958 · Cited by 12
Peric, D., Chvalova, K., & Rousselet, G. (2011) · Oncogene · doi:10.1038/onc.2011.391 · Cited by 14
“This global approach allowed to circumvent the often silent phenotype observed after inhibition of individual micro-RNAs (Miska et al., 2007; Wang et al., 2008), a probable consequence of the structural and functional redundancy of these regulatory RNAs.”
BackgroundA Potential of microRNAs for High-Content Screening
Serva, A., Claas, C., & Starkuviene, V. (2011) · Journal of Nucleic Acids · doi:10.4061/2011/870903 · Cited by 13
“elegans are individually dispensable [161], and Voorhoeve et al.”
BackgroundXu, W., Liu, J., Qi, H., Si, R., Zhao, Z., Tao, Z., Bai, Y., Hu, S., Sun, X., Cong, Y., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-47055-4 · Cited by 14
“8, and Supplementary Data 8), thus highlighting the utility of cellular resolution expression analysis.”
InfluentialBejarano, F., Chang, C.-H., Sun, K., Hagen, J. W., Deng, W., & Lai, E. C. (2021) · Developmental Biology · doi:10.1016/j.ydbio.2021.02.010 · Cited by 12
Genomic non-redundancy of the mir-183/96/182 cluster and its requirement for hair cell maintenance
Fogerty, J., Stepanyan, R., Cianciolo, L. T., Tooke, B. P., & Perkins, B. D. (2019) · Scientific Reports · doi:10.1038/s41598-019-46593-y · Cited by 11
Felden, B., & Gilot, D. (2018) · Genes · doi:10.3390/genes10010022 · Cited by 15
“Similar findings have been reported in Caenorhabditis elegans [79,80] and in plants [81].”
ResultMapping the Pax6 3’ untranslated region microRNA regulatory landscape
Ryan, B. C., Lowe, K., Hanson, L., Gil, T., Braun, L., Howard, P. L., & Chow, R. L. (2018) · BMC Genomics · doi:10.1186/s12864-018-5212-x · Cited by 9
The role of micro RNA s in Anopheles biology—an emerging research field
Lampe, L., & Levashina, E. A. (2017) · Parasite Immunology · doi:10.1111/pim.12405 · Cited by 12
Argonaute protein as a linker to command center of physiological processes.
Wei, K., Wu, L. J., Chen, Y., Lin, Y., Wang, Y., Liu, X., & Xie, D. (2013) · Europe PMC (PubMed Central) · doi:10.3978/j.issn.1000-9604.2013.08.13 · Cited by 11
Robustness of the hypoxic response: Another job for miRNAs?
Ezcurra, A. L. D. L., Bertolin, A. P., Melani, M., & Wappner, P. (2012) · Developmental Dynamics · doi:10.1002/dvdy.23865 · Cited by 11
“Moreover, in general, individual miRNA knock-out animals don’t display dramatic phenotypes under controlled laboratory conditions (Li and Carthew, 2005; Miska et al., 2007; Li et al., 2009; Alvarez-Saavedra and Horvitz, 2010).”
BackgroundmiR-11 regulates pupal size of Drosophila melanogaster via directly targeting Ras85D.
Li, Y., Li, S.-J., Jin, P., Chen, L.-M., & Ma, F. (2017) · American Journal of Physiology - Cell Physiology · doi:10.1152/ajpcell.00190.2016 · Cited by 11
“The absence of strong loss-of-function phenotypes of a large proportion of miRNA mutants and considerable redundancy among miRNAs of the same family in gene regulation make it difficult to identify miRNA target genes and characterize the functions of an individual miRNA (25).”
BackgroundIdentification of miRNAs and their targets in C. elegans.
Lima, S., & Pasquinelli, A. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-1221-6_12 · Cited by 11
Sandovici, I., Fernandez‐Twinn, D. S., Campbell, N., Cooper, W. N., Sekita, Y., Zvetkova, I., Ferland-McCollough, D., Prosser, H. M., Oyama, L. M., Pantaleão, L. C., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114750 · Cited by 12
The Significance of MicroRNAs in the Molecular Pathology of Brain Metastases
Siegl, F., Večeřa, M., Rošková, I., Smrčka, M., Jančálek, R., Kazda, T., Slabý, O., & Šáňa, J. (2022) · Cancers · doi:10.3390/cancers14143386 · Cited by 15
“elegans did not cause essential dysfunction in development or viability; just 10% miRNA was sufficient to maintain the normal phenotype of the organism [81].”
BackgroundMedley, J. C., Hebbar, S., Sydzyik, J. T., & Zinovyeva, A. (2021) · Genetics · doi:10.1093/genetics/iyab199 · Cited by 9
“As a result of sharing the same seed sequence, many members of microRNA families often exhibit functional redundancy with other family members (Abbott et al. 2005; Miska et al. 2007; Alvarez-Saavedra and Horvitz 2010).”
Inamura, N., Go, S., Watanabe, T., Takase, H., Takakura, N., Nakayama, A., Takebayashi, H., Matsuda, J., & Enokido, Y. (2021) · Brain Pathology · doi:10.1111/bpa.12951 · Cited by 11
“Although loss- of- function mutations of the majority of individual miRNAs cause no overt developmental defects in many organisms (30), genetic deletion of miR219 leads to defective OL development and high susceptibility to the experimentally induced demyelinating lesions (13).”
BackgroundExploring the miRNA Regulatory Network Using Evolutionary Correlations
Obermayer, B., & Levine, E. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003860 · Cited by 11
“many of the hundreds of miRNAs discovered ever since [23–25].”
BackgroundNot miR ‐ly micromanagers: the functions and regulatory networks of microRNAs in mammalian skin
Riemondy, K. A., Hoefert, J. E., & Yi, R. (2014) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1250 · Cited by 8
Pleiotropic Constraints, Expression Level, and the Evolution of miRNA Sequences
Jovelin, R. (2013) · Journal of Molecular Evolution · doi:10.1007/s00239-013-9588-6 · Cited by 10
“elegans miRNAs do not cause large phenotypic abnormalities, suggesting functional redundancy among miRNAs (Miska et al. 2007) and/ or subtle phenotypic effects that require fine-grained analyses (Abbott 2010; Ramani et al.”
Roles of microRNAs in the Caenorhabditis elegans nervous system.
Meng, L.-F., Chen, L., Li, Z.-Y., Wu, Z.-X., & Ge, S. (2013) · Journal of genetics and genomics = Yi chuan xue bao · doi:10.1016/j.jgg.2013.07.002 · Cited by 10
'Inc-miRs': functional intron-interrupted miRNA genes.
Zhang, H., Maniar, J. M., & Fire, A. (2011) · Genes & Development · doi:10.1101/gad.2058711 · Cited by 10
Non-coding RNAs in Complex Diseases
Li, X., Xiao, Y., Ning, S.-W., & Zhang, Y.-P. (2018) · Advances in Experimental Medicine and Biology · doi:10.1007/978-981-13-0719-5 · Cited by 10
“For example, the lncRNA HOTAIR serves as an endogenous “sponge” of miR-141, resulting in significant reduction of glioma growth [5].”
BackgroundInfluentialDetection of features predictive of microRNA targets by integration of network data
Cihan, M., & Andrade, M. (2022) · PLoS ONE · doi:10.1371/journal.pone.0269731 · Cited by 9
“However, miRNA functional characterization is experimentally difficult due to their regulatory mechanisms, which are more subtle and less specific than transcription factors and epigenetic modifications [8].”
BackgroundMathematics of microRNAs: stabilizing gene regulatory networks
Ambros, V. (2019) · National Science Review · doi:10.1093/nsr/nwz112 · Cited by 9
Self-citationmir-234 controls neuropeptide release at the Caenorhabditis elegans neuromuscular junction.
Snieckute, G., Baltaci, O. F., Liu, H.-W., Li, L., Hu, Z.-T., & Pocock, R. (2019) · Molecular and cellular neurosciences · doi:10.1016/j.mcn.2019.06.001 · Cited by 9
microRNAs selectively protect hub cells of the germline stem cell niche from apoptosis
Volin, M., Zohar-Fux, M., Gonen, O., Porat‐Kuperstein, L., & Toledano, H. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201711098 · Cited by 11
“These results are in line with previous findings, indicating that individual miRNAs are not essential for viability (Miska et al., 2007).”
ResultGrosswendt, S., & Rajewsky, N. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804402-5.00002-9 · Cited by 7
Jovelin, R., & Cutter, A. (2016) · Worm · doi:10.1080/21624054.2016.1156835 · Cited by 8
miRNA regulation in the context of functional protein networks: principles and applications
Alshalalfa, M. (2014) · Wiley Interdisciplinary Reviews: Systems Biology and Medicine · doi:10.1002/wsbm.1251 · Cited by 8
“37 A miRNA downregulates its targets, thus negative correlation in expression levels between a miRNA and its direct targets indicates that the miRNA is functional.”
BackgroundMicroRNAs that interfere with RNAi
Massirer, K., & Pasquinelli, A. (2013) · Worm · doi:10.4161/worm.21835 · Cited by 8
MicroRNAs Add an Additional Layer to the Complexity of Cell Signaling
Herschkowitz, J. I., & Fu, X. (2011) · Science Signaling · doi:10.1126/scisignal.2002182 · Cited by 8
“Yet, genetic analysis in Caenorhabiditis elegans showed that only 10% of individual miRNA knockouts led to clear developmental or morphological defects (9).”
BackgroundMookherjee, S., Sinha, M., Mukhopadhyay, S., Bhattacharyya, N. P., & Mohanty, P. K. (2009) · arXiv (Cornell University) · doi:10.48550/arxiv.0901.4211 · Cited by 5
Quesnelle, D. C., Bendena, W. G., & Chin-Sang, I. D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24086963 · Cited by 9
“Mir-51 family members belong to the highly conserved mir-100 family of miRNAs and, as observed in mir-35 family mutants, exhibit high levels of redundancy [82,95,96].”
BackgroundChaya, T., Maeda, Y., Sugimura, R., Okuzaki, D., Watanabe, S., Varner, L. R., Motooka, D., Gyoten, D., Yamamoto, H., Kato, H., et al. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102293 · Cited by 9
“elegans miR-124 mutants, neurons are normally generated and no overt phenotype is observed (3, 4).”
BackgroundMicroRNAs Regulate Multiple Aspects of Locomotor Behavior inDrosophila
Donelson, N. C., Dixit, R., Pichardo‐Casas, I., Chiu, E. Y., Ohman, R. T., Slawson, J. B., Klein, M., Fulga, T. A., Vactor, D. V., & Griffith, L. C. (2019) · G3 Genes Genomes Genetics · doi:10.1534/g3.119.400793 · Cited by 9
Pucella, J. N., Cols, M., Yen, W.-F., Xu, S., & Chaudhuri, J. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1800071 · Cited by 9
“Systematic knockout of individual miRNAs, expected to unveil a bounty of developmental phenotypes, revealed startlingly few phenotypes (62, 63).”
BackgroundSimilarity in targets with REST points to neural and glioblastoma related miRNAs
Gebhardt, M. L., Reuter, S., Mrowka, R., & Andrade-Navarro, M. A. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku231 · Cited by 6
“There may be multiple reasons for this: miRNAs only have an impact on the regulation of genes that have already been transcribed, therefore acting further downstream than TFs; co-regulation of the same transcript by multiple miRNAs is common and therefore the effect of loss of one miRNA might not have a big impact (6,…”
BackgroundExpression Pattern Analysis of MicroRNAs in Caenorhabditis elegans
Isik, M., & Berezikov, E. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-083-0_11 · Cited by 7
Sharma, D. R., Rödelsperger, C., Röseler, W., Witte, H., Werner, M. S., & Sommer, R. J. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.19.604269 · Cited by 6
“5E-H)(Miska et al. , 2007; Alvarez-Saavedra and Horvitz, 2010).”
Fish models to explore epigenetic determinants of hypoxia-tolerance
Johnston, W., Adil, S., Cao, C., Nipu, N., & Mennigen, J. A. (2025) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2025.111811 · Cited by 9
Lee, J., Hong, I., Lee, C., Kim, D., Kim, S., & Lee, Y. (2024) · Scientific Reports · doi:10.1038/s41598-024-61673-4 · Cited by 4
“Additionally, deletion of a single miRNA may cause phenotypic changes because of the complex and highly regulated network of interactions between miRNAs and mRNAs within the genetic network 15,16 .”
BackgroundmiRNA suppression of a Notch repressor directs non-neuronal fate in Drosophila mechanosensory organs
Kavaler, J., Duan, H., Aradhya, R., de Navas, L. F., Joseph, B. J., Shklyar, B., & Lai, E. C. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201706101 · Cited by 6
“Conservation of miRNA function via divergent targets: antineural activity of mir-279/996 The vast majority of miRNA knockouts in diverse animals reveal mostly subtle and/or impenetrant defects, especially during the course of normal development (Miska et al., 2007; Chen et al., 2014).”
BackgroundZabinsky, R. A., Weum, B., Cui, M., & Han, M. (2017) · G3 Genes Genomes Genetics · doi:10.1534/g3.117.043414 · Cited by 6
Rissland, O. S., & Lai, E. C. (2011) · Development · doi:10.1242/dev.065284 · Cited by 8
“In contrast to mutants of the founding miRNAs lin-4 and let-7, many MEETING REVIEW Development 138 (15) D E V E LO P M E N T 3097MEETING REVIEWDevelopment 138 (15) other individual miRNA mutants lack obvious phenotypes (Miska et al., 2007).”
BackgroundFunctional genomic, computational and proteomic analysis of C. elegans microRNAs
Lehrbach, N. J., & Miska, E. A. (2008) · Briefings in Functional Genomics and Proteomics · doi:10.1093/bfgp/eln024 · Cited by 7
“elegansmiRNAs are currently available [35].”
Self-citationGeneration of 3′UTR knockout cell lines by CRISPR/Cas9-mediated genome editing
Mitschka, S., Fansler, M. M., & Mayr, C. (2021) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2021.03.014 · Cited by 10
MicroRNAs in Drosophila Cancer Models
Sander, M., & Herranz, H. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-23629-8_9 · Cited by 9
The rapidly evolving X-linked MIR-506 family fine-tunes spermatogenesis to enhance sperm competition
Wang, Z., Wang, Y., Zhou, T., Chen, S., Morris, D., Magalhães, R. D. M., Li, M., Wang, S., Wang, H., Xie, Y., et al. (2024) · eLife · doi:10.7554/elife.90203 · Cited by 8
“…with previous efforts to inactivate miRNA genes in Caenorhabditis elegans and mice ( Wang et al., 2020b ; Bao et al., 2012 ; Wang et al., 2022 ; Miska et al., 2007 ), KOs of either individual members or individual clusters of the MIR-506 family induced no discernible phenotypes and did not…”
BackgroundEDC-3 and EDC-4 Regulate Embryonic mRNA Clearance and Biomolecular Condensate Specialization
Vidya, E., Jami-Alahmadi, Y., Mayank, A., Rizwan, J., Xu, J., Cheng, T., Leventis, R., Sonenberg, N., Wohlschlegel, J., Vera, M., et al. (2024) · bioRxiv · doi:10.1101/2024.03.04.583404 · Cited by 5
Ruediger, C. T., Karimzadegan, S., Lin, S., & Shapira, M. (2021) · Genetics · doi:10.1093/genetics/iyab049 · Cited by 5
A deeply conserved miR-1 dependent regulon supports muscle cell physiologyPreprint
Gutiérrez‐Pérez, P., Santillán, E. M., Lendl, T., Schrempf, A., Steinacker, T. L., Asparuhova, M., Brandstetter, M., Haselbach, D., & Cochella, L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.31.275644 · Cited by 4
Iftikhar, H., Schultzhaus, J. N., Bennett, C. J., & Carney, G. E. (2017) · RNA Biology · doi:10.1080/15476286.2016.1272748 · Cited by 5
Twists and turns—How we stepped into and had fun in the “boring” lipid field
Han, M. (2015) · Science China Life Sciences · doi:10.1007/s11427-015-4949-6 · Cited by 5
Discerning Different In vivo Roles of MicroRNAs by Experimental Approaches in Zebrafish
Pase, L. B., & Lieschke, G. J. (2011) · Methods in cell biology · doi:10.1016/b978-0-12-374814-0.00020-3 · Cited by 5
Joughin, B. A., Cheung, E. C. W., Karuturi, R. K. M., Sáez-Rodríguez, J., Lauffenburger, D. A., & Liu, E. T. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-372550-9.00004-3 · Cited by 3
Initial function of microRNAs as a defence mechanism against invading organisms
Liu, X., Zang, X., Feng, H., Zhao, Q., Zhang, C., & Wang, J. (2019) · ExRNA · doi:10.1186/s41544-019-0018-9 · Cited by 4
“are not essential for organismal viability [12].”
BackgroundTag team: Roles of microRNAs and proteolytic regulators in ensuring robust gene expression dynamics
Weaver, B. P., & Han, M. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.09.009 · Cited by 4
“elegans, many individual miRNAs were shown to be non-essential [1] and even entire families of miRNAs were shown to be non-essential [2].”
BackgroundErnsberger, U. (2015) · Cell and Tissue Research · doi:10.1007/s00441-015-2187-7 · Cited by 4
Functional analysis of the miRNA-mRNA interaction network in C. elegans
Than, M. T., & Han, M. (2013) · Worm · doi:10.4161/worm.26894 · Cited by 4
Murphy, C. (2010) · Current Biology · doi:10.1016/j.cub.2010.11.018 · Cited by 4
“Previous studies had not uncovered any obvious developmental phenotypes for the miRNAs in question [10]; de Lencastre et al.”
BackgroundThe Drosophila Model in Cancer
Deng, W.-M. (2019) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-030-23629-8 · Cited by 4
Knittel, T. L., Montgomery, B. E., Reed, K. J., Chong, M. C., Isolehto, I. J., Cafferty, E. R., Smith, M. J., Sprister, R. A., Magelky, C. N., Scherman, H., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-60721-5 · Cited by 5
“Thistolerance might explain why the loss of most individual miRNAs does not result in strong developmental defects 32 .”
MicroRNAs are necessary for the emergence of Purkinje cell identity
Zolboot, N., Xiao, Y., Du, J. X., Ghanem, M. M., Choi, S. Y., Junn, M. J., Zampa, F., Huang, Z., MacRae, I. J., & Lippi, G. (2023) · bioRxiv · doi:10.1101/2023.09.28.560023 · Cited by 3
“While knocking out individual miRNAs in nematodes rarely leads to measurable phenotypes 1,2 , it has progressively more severe consequences from flies 3 to zebrafish 4,5 to mice 6 .”
BackgroundMicromanaging pattern formation: miRNA regulation of signaling systems in vertebrate development
Copeland, J., Wilson, K. E., & Simões-Costa, M. (2021) · FEBS Journal · doi:10.1111/febs.16139 · Cited by 3
Systematic comparison of the response properties of protein and RNA mediated gene regulatory motifs.
Iyengar, B. R., Pillai, B., Venkatesh, K., & Gadgil, C. J. (2017) · Molecular Biosystems · doi:10.1039/c6mb00808a · Cited by 3
Davidson, E. H., & Peter, I. S. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-404729-7.00001-0 · Cited by 6
MicroRNA modulation of caenorhadbitis elegans dietary restriction and longevity
Vora, M. (2011) · Rutgers University Community Repository (Rutgers University) · doi:10.7282/t3z31xqs
Regulation of microRNA activity in stress
Funikov, S. Y., & Zatcepina, O. G. (2017) · Molecular Biology · doi:10.1134/s0026893317030050 · Cited by 7
McIlhargey, F. K., Vandervelden, J. E., Sabry, R., & Favetta, L. A. (2026) · Reproductive Toxicology · doi:10.1016/j.reprotox.2026.109270 · Cited by 2
Argonautes and small RNAs associated with nematode programmed DNA elimination
Zagoskin, M., Kang, Y.-Y., Davis, R. E., & Wang, J.-B. (2025) · bioRxiv · doi:10.1101/2025.10.23.684123 · Cited by 2
The Multifaceted Role of miR-211 in Health and Disease
Parra, J. R., Grand, Z., Gonzalez, G., Perera, R. J., Pandeya, D. R., Weiler, T., & Chapagain, P. P. (2025) · Biomolecules · doi:10.3390/biom15081109 · Cited by 2
“These small RNAs regulate gene expression by repressing translation or inducing the degradation of messenger RNAs (mRNAs) across a wide range of species. miRNAs were first discovered in 1993 during experiments on the nematode, Caenorhabditis elegans [1].”
In vivo AGO-APP identifies a module of microRNAs cooperatively preserving neural progenitors
Narbonne-Reveau, K., Erni, A., Eichner, N., Sankar, S. H. H., Surbhi, S., Meister, G., Cremer, H., Maurange, C., & Béclin, C. (2025) · PLoS Genetics · doi:10.1371/journal.pgen.1011680 · Cited by 3
“Moreover, loss of specific miRNAs induces generally only minimal changes in target gene expression [10,11] and often only mild to absent phenotypes [12,13], complicating functional analysis.”
The mex-3 3’ untranslated region is essential for reproduction during temperature stress
Brown, H. E., Varderesian, H. V., Keane, S. A., & Ryder, S. P. (2024) · bioRxiv · doi:10.1101/2024.04.01.587367 · Cited by 2
“Specifically, microRNAs (miRNAs) that repress key hetero-chronic pathway mRNA targets during larval development rarely have a phenotype when mutated (Alvarez-Saavedra and Horvitz, 2010; Miska et al., 2007).”
Tarbier, M., Mackowiak, S. D., Sekar, V., Bonath, F., Yapar, E., Fromm, B., Faridani, O. R., Biryukova, I., & Friedländer, M. R. (2026) · Genome Research · doi:10.1101/gr.279914.124 · Cited by 1
“The hypothesis that miRNAs buffer gene expression noise fits well with observations that many mutant animals that are devoid of specific miRNAs do not display obvious phenotypes under laboratory conditions but only when subjected to stress conditions (Miska et al. 2007; Li et al. 2009).”
A nonneural miRNA cluster mediates hearing via repression of two neural targetsPreprint
Zhang, B., Duan, H., Kavaler, J., Lu, W., Eberl, D. F., & Lai, E. C. (2023) · Genes & Development · doi:10.1101/gad.351052.123 · Cited by 2
“…miRNAs (Lee et al. 1993; Reinhart et al. 2000), miRNA genes are generally dispensable for gross aspects of development, viability, or physiology (Miska et al. 2007; Alvarez-Saavedra and Horvitz 2010; Park et al. 2012; Chen et al. 2014) and have often been considered either to be used for…”
Chipman, L. B., Luc, S., Nicastro, I. A., Hulahan, J. J., Dann, D. C., Bodas, D. M., & Pasquinelli, A. E. (2023) · PLoS Genetics · doi:10.1371/journal.pgen.1011055 · Cited by 2
An integrin binding motif in TLN-1/talin plays a minor role in motility and ovulation
Sadeghian, F., Ibrahim, I., Ravichandran, L., Henderson, G., Acharya, A., Wang, L., Lee, M., & Cram, E. (2023) · microPublication Biology · doi:10.17912/micropub.biology.000726 · Cited by 2
“Although the tln-1 null phenotype is not known, a deletion allele n4099 (which also removes mir-50) is inviable (Miska et al., 2007).”
BackgroundMicroRNA-27a is essential for bone remodeling by modulating p62-mediated osteoclast signaling
Wang, S., Maruyama, E. O., Martinez, J. C., Lopes, J., Hsu, T., Wu, W., Hsu, W., & Maruyama, T. (2022) · bioRxiv · doi:10.1101/2022.06.13.495939 · Cited by 2
The FGFR4 Homolog KIN-9 Regulates Lifespan and Stress Responses in Caenorhabditis elegans
Mallick, A., Xu, L., Mehta, S., Taylor, S. K. B., Hosein, H., & Gupta, B. (2022) · Frontiers in Aging · doi:10.3389/fragi.2022.866861 · Cited by 2
“We assessed the transcript levels of top three potential targets (cah-4, kin-9, and pbs-5) in an miR-246 deletion mutant that lacks the entire transcript and 5ʹ upstream sequence (n4636: 518 bp length) (Miska et al., 2007) (Figures 1A,B).”
MethodIntergenerational pathogen-induced diapause in C. elegans is modulated by mir-243Preprint
Gabaldón, C., Legüe, M., Palominos, M. F., Verdugo, L., Gutzwiller, F., & Calixto, A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.31.019349 · Cited by 3
Connecting the molecular function of microRNAs to cell differentiation dynamics
Posner, R., & Laubenbacher, R. (2019) · Journal of The Royal Society Interface · doi:10.1098/rsif.2019.0437 · Cited by 5
“For example, most knockouts of one or several miRNAs in C. elegans have been shown to produce no developmental or phenotypic abnormalities [14,15].”
BackgroundXu, Y., Chen, Y., Li, D., Liu, Q., Xuan, Z., & Li, W.-H. (2016) · RNA Biology · doi:10.1080/15476286.2016.1270006 · Cited by 2
Winslow, R. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00107 · Cited by 2
A growing molecular toolbox for the functional analysis of microRNAs in Caenorhabditis elegans
Jo, J., & Esquela‐Kerscher, A. (2011) · Briefings in Functional Genomics · doi:10.1093/bfgp/elr012 · Cited by 2
“types reported in animals genetically deleted for miR-237 [25] and demonstrating the high specificity”
Eukaryotic Evolution: The Importance of Being Archaebacterial
Logsdon, J. M., Jr. (2010) · Current Biology · doi:10.1016/j.cub.2010.11.020 · Cited by 2
Le monde complexe et mouvant des ARN. Seconde partie : les microARNs
Lamoril, J., Bouizegarène, P., & Bogard, M. (2010) · Immuno-analyse & Biologie Spécialisée · doi:10.1016/j.immbio.2010.07.003 · Cited by 3
Robust and specific inhibition of microRNAs in Caenorhabditis elegans
Kundu, S., & Slack, F. (2010) · Journal of Biology · doi:10.1186/jbiol230 · Cited by 2
MicroRNAs in Therapy and Toxicity
MacEwan, D., Shah, N. M., & Antoine, D. (2017) · doi:10.1007/978-1-4939-6743-8_10 · Cited by 2
Ying, S. (2013) · Methods in Molecular Biology · doi:10.1007/978-1-62703-083-0 · Cited by 2
Feng, S., Pei, Y.-W., Gao, X., Yang, D.-J., Liu, J., Guo, Z., Zhang, Z.-D., & Zhou, L. (2026) · Animals · doi:10.3390/ani16152434 · Cited by 1
“Conversely, a single mRNA (such as CXXC4 ) is often subject to combinatorial regulation by multiple endogenous miRNAs, a functional redundancy evidenced by the fact that many miRNAs are dispensable for baseline organismal viability [45].”
Metadata
- Authors
- Miska, E. A., Alvarez-Saavedra, E., Abbott, A. L., Lau, N. C., Hellman, A. B., McGonagle, S. M., Bartel, D. P., Ambros, V. R., & Horvitz, H. R.
- Affiliations
- Howard Hughes Medical Institute (US)
- Whitehead Institute for Biomedical Research (US)
- Corresponding author
- Horvitz, H. Robert
- ORCID
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2007-12-14
- Volume
- 3
- Issue
- 12
- Pages
- e215
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC2134938
- OpenAlex
- W2003952411
- Cited by
- 484
- References
- 111
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 17 · 2023: 14 · 2022: 12 · 2021: 15 · 2020: 16 · 2019: 21 · 2018: 24 · 2017: 28 · 2016: 29 · 2015: 33 · 2014: 46 · 2013: 39 · 2012: 60
- FWCI
- 9.91
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- e-Publications@Marquette (Marquette University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Ellison Medical Foundation
- Wellcome Trust (061641)
- National Institutes of Health (5f32gm065721-03)
- National Institute of General Medical Sciences (GM067031, R01GM067031, 5F32GM065721-02, GM34028, R01GM034028, F32 GM065721)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Keywords
- microRNA, Caenorhabditis elegans, post-transcriptional regulation
- MeSH terms
- Animals, Mutation, Phenotype, Conserved Sequence, Caenorhabditis elegans, Genes, Helminth, Sequence Deletion, RNA, Helminth, Evolution, Molecular, MicroRNAs
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
