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Ribosome Profiling Shows That miR-430 Reduces Translation Before Causing mRNA Decay in Zebrafish
Open accessAbstract
Translation Block: MicroRNAs (miRNAs) are small, noncoding RNA genes that are found in the genomes of most eukaryotes, where they play an important role in the regulation of gene expression. Although whether gene activity is repressed by blocking translation of messenger RNA (mRNA) targets, or by promoting their deadenylation and then degradation, has been open to debate. Bazzini et al. (p. 233 , published online 15 March) and Djuranovic et al. (p. 237 ) looked at early points in the repression reaction in the zebrafish embryo or in Drosophila tissue culture cells, respectively, and found that translation was blocked before target mRNAs were significantly deadenylated and degraded. Thus, miRNAs appear to interfere with the initiation step of translation.
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“miRNAs are excised from larger stem-loop-containing transcripts and are subsequently incorporated into argonaute (Ago) proteins. This generates functional entities capable of silencing target transcripts via translational repression and mRNA destabilization (Bazzini et al., 2012; Djuranovic et al., 2012).”
From Transcriptome-wide Discovery of microRNA Binding Sites in Human Brain (2014) · cites this paper as Bazzini et al., 2012
Experimental — accuracy not yet measuredIn the citing paper
“Global measurements indicate that miRNA targeting causes mostly mRNA destabilization, with translational repression comprising a detectable but minor component of the overall repression33–36.”
From Poly(A)-tail profiling reveals an embryonic switch in translational control (2014) · cites this paper as [36]
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“The only known exception is the transient translational repression observed in early zebrafish embryos36.”
From Poly(A)-tail profiling reveals an embryonic switch in translational control (2014) · cites this paper as [36]
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“At 4 hpf miR-430 targeting causes mostly translational repression with very little mRNA destabilization, whereas by 6 hpf the outcome shifts to mostly mRNA destabilization36.”
From Poly(A)-tail profiling reveals an embryonic switch in translational control (2014) · cites this paper as [36]
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Small but sturdy: small RNAs in cellular memory and epigeneticsPreprint
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BackgroundNew technologies accelerate the exploration of non-coding RNAs in horticultural plants
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Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish
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“Other variations of the PAT assay include enzymatic G-tailing (Kusov et al., 2001) or G/I-tailing (Bazzini et al., 2012) of the 30 end.”
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“However, it has been proposed that this fateful and irreversible miRNA-mediated effect on cellular mRNAs is often preceded by transient translational repression, which sometimes may also occur independent of mRNA degradation.(4,60,63) Multiple models have been proposed to explain miRNA-mediated translational repressio…”
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BackgroundThe Sequence and Structure Determine the Function of Mature Human miRNAs
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“Silencing occurs via endonucleolytic cleavage, or “slicing” (Baumberger & Baulcombe, 2005) and/or translational repression possibly coupled to accelerated mRNA decay (Brodersen et al , 2008; Guo et al , 2010; Bazzini et al , 2012; Li et al , 2013).”
RNA ‐based mechanisms regulating host–virus interactions
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“For targets with partial complementarity, silencing is initially primed through translational repression and followed by mRNA destabilization (Bazzini et al., 2012; Djuranovic et al., 2012).”
Genome‐scale, single‐cell‐type resolution of microRNA activities within a whole plant organ
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“In zebrafish, miR-430 alone operates the clearance of hundreds of maternally deposited zygotic transcripts via TR followed by mRNA decay shortly after fertilization, to ensure proper morphogenesis (Giraldez et al , 2006; Bazzini et al , 2012).”
Overview of MicroRNAs as Diagnostic and Prognostic Biomarkers for High-Incidence Cancers in 2021
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“Three papers published in 2012 provided insights into the dynamics of miRNA-mediated repression in fly, zebrafish, and human cells (Bazzini et al., 2012; Bethune et al., 2012; Djuranovic et al., 2012).”
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“miRNAs can inhibit the extension or termination of translation or degrade newly synthesized peptide chains from ribosomes (Bazzini et al., 2012).”
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“In contrast, application of ribosome profiling by Bazzini et al. (2012) to examine broad miR-430-dependent repression of expression in zebrafish embryos suggested that miR-430 regulation in this context results in inhibition of translation that precedes mRNA decreases.”
BackgroundMicroRNAs Establish Uniform Traits during the Architecture of Vertebrate Embryos
Kasper, D. M., Moro, A., Ristori, E., Narayanan, A., Hill-Terán, G., Fleming, E. S., Moreno-Mateos, M. A., Vejnar, C. E., Zhang, J., Lee, D., et al. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.02.021 · Cited by 54
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“This finding is relevant given the conflicting reports about the predominant mechanism and order of repression mechanisms [37] that are utilized by miRNAs to modulate gene expression, whether that be mRNA level repression [38] or translation inhibition [39,40].”
BackgroundAUF1 facilitates microRNA-mediated gene silencing
Min, K., Jo, M. H., Shin, S., Davila, S., Zealy, R. W., Kang, S. I., Lloyd, L. T., Hohng, S., & Yoon, J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx149 · Cited by 57
“Correlations between miRNA and mRNA expression in steady state reveal that increased miRNA levels do not always lead to changes in the levels of all target mRNAs (18,19).”
BackgroundRNA tales – how embryos read and discard messages from mom
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“The latter findings agree with previous reports of delayed degradation of mRNAs with AREs in Xenopus, and miRNA targets in zebrafish embryos (Voeltz and Steitz, 1998; Bazzini et al., 2012; Subtelny et al., 2014).”
BackgroundResultTED-Seq Identifies the Dynamics of Poly(A) Length during ER Stress
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“Upon association with AGO, the miRNA then guides RISC to target mRNAs via partial sequence complementarity, which results in translational repression and mRNA turnover (Bazzini et al. 2012; Djuranovic et al. 2012).”
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“Binding of miRNAs in RISC to a specific mRNA transcript, negatively regulates gene expression by either reducing translational efficiency or by promoting mRNA degradation [6,7,8].”
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“To validate the Poly(A)-seq detected poly(A) tails, we applied the Affymetrix poly(A) length assay kit based on high resolution poly(A) tail (Hire-PAT) assay [32].”
MethodBrosnan, C. A., Palmer, A., & Zuryn, S. (2021) · Nature Communications · doi:10.1038/s41467-021-22503-7 · Cited by 56
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Single-molecule imaging of microRNA-mediated gene silencing in cells
Kobayashi, H., & Singer, R. H. (2022) · Nature Communications · doi:10.1038/s41467-022-29046-5 · Cited by 59
Editorial focus: entering into the non-coding RNA era
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Translation regulation gets its ‘omics’ moment
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Rapid and specific purification of Argonaute-small RNA complexes from crude cell lysates
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“2010) and, in some cases, repressing their translation into protein (Hendrickson et al. 2009; Bazzini et al. 2012).”
Wu, L., Lv, Y., Ye, Y., Liang, Y., & Ye, J. (2020) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.0c03341 · Cited by 51
Functional Mapping of the Zebrafish Early Embryo Proteome and Transcriptome
Shaik, A. A., Wee, S., Li, R. H. X., Li, Z., Carney, T. J., Mathavan, S., & Gunaratne, J. (2014) · Journal of Proteome Research · doi:10.1021/pr5005136 · Cited by 47
MicroRNA Target Identification—Experimental Approaches
Martínez-Sánchez, A., & Murphy, C. L. (2013) · Biology · doi:10.3390/biology2010189 · Cited by 56
“Nevertheless, using a similar technique, Bazzani and co-workers [66] found that the effects of miR-430 in zebrafish occur at the level of translation preceding RNA decay, so this disparity may result from the steady-state conditions used, the biological system, or the miRNA under study.”
Cotranslational microRNA mediated messenger RNA destabilization
Tat, T. T., Maroney, P. A., Chamnongpol, S., Coller, J., & Nilsen, T. W. (2016) · eLife · doi:10.7554/elife.12880 · Cited by 50
Endogenous miRNA in the green alga Chlamydomonas regulates gene expression through CDS-targeting
Chung, B., Deery, M. J., Groen, A. J., Howard, J., & Baulcombe, D. C. (2017) · Nature Plants · doi:10.1038/s41477-017-0024-6 · Cited by 50
PTRE-seq reveals mechanism and interactions of RNA binding proteins and miRNAs
Cottrell, K. A., Chaudhari, H. G., Cohen, B. A., & Djuranović, S. (2018) · Nature Communications · doi:10.1038/s41467-017-02745-0 · Cited by 51
Regulation and different functions of the animal microRNA‐induced silencing complex
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“The fact that this complex is not interacting with the deadenylation machinery suggests that it might have an alternative function such as early translation inhibition preceding mRNA decay as reported in zebrafish embryos (Bazzini et al., 2012).”
BackgroundA Dicer-miR-107 Interaction Regulates Biogenesis of Specific miRNAs Crucial for Neurogenesis
Ristori, E., Lopez‐Ramirez, M. A., Narayanan, A., Hill-Terán, G., Moro, A., Calvo, C., Thomas, J., & Nicoli, S. (2015) · Developmental Cell · doi:10.1016/j.devcel.2014.12.013 · Cited by 54
“Micro-RNAs (miRNAs) are highly conserved noncoding small RNAs that bind to the 30UTR of target messenger RNAs (mRNAs) and posttranscriptionally regulate the expression of genes by repressing translation and/or decreasing transcript stability (Bazzini et al., 2012; Guo et al., 2010).”
BackgroundModulation of Epigenetic Regulators and Cell Fate Decisions by miRNAs
Gruber, A. J., & Zavolan, M. (2013) · Epigenomics · doi:10.2217/epi.13.65 · Cited by 48
The influence of microRNAs and poly(A) tail length on endogenous mRNA–protein complexes
Rissland, O. S., Subtelny, A. O., Wang, M., Lugowski, A., Nicholson, B. L., Laver, J. D., Sidhu, S. S., Smibert, C. A., Lipshitz, H. D., & Bartel, D. P. (2017) · Genome biology · doi:10.1186/s13059-017-1330-z · Cited by 52
“Interestingly, there are specific developmental contexts, such as in the pre-gastrulation fish embryo, where deadenylation, rather than stimulating decapping, leads to robust translational repression [35, 36].”
BackgroundA common variant alters SCN5A–miR-24 interaction and associates with heart failure mortality
Zhang, X., Yoon, J., Morley, M. P., McLendon, J. M., Mapuskar, K. A., Gutmann, R. A., Mehdi, H., Bloom, H. L., Dudley, S. C., Ellinor, P. T., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci95710 · Cited by 50
Transcriptome-wide measurement of ribosomal occupancy by ribosome profiling
Aeschimann, F., Xiong, J., Arnold, A. W., Dieterich, C., & Großhans, H. (2015) · Methods · doi:10.1016/j.ymeth.2015.06.013 · Cited by 49
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“5) also were performed by studying poly(A ) mRNA, suggesting miRNA-directed deadenylation, in keeping with other reports (1, 54).”
ResultDUSP11 – An RNA phosphatase that regulates host and viral non-coding RNAs in mammalian cells
Burke, J. M., & Sullivan, C. S. (2017) · RNA Biology · doi:10.1080/15476286.2017.1306169 · Cited by 47
“RISC generally represses gene expression of the mRNA by direct cleavage of the mRNA(20) or by repression of translation followed by increased turnover of the mRNA.(21,22) Small interfering RNAs”
BackgroundAssessing the translational landscape of myogenic differentiation by ribosome profiling
de Klerk, E., Fokkema, I. F. A. C., Thiadens, K. A. M. H., Goeman, J. J., Palmblad, M., den Dunnen, J. T., Lindern, M. V., & Hoen, P. A. C. ’. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv281 · Cited by 47
“Recent studies based on ribosome footprint profiling have reported extensive regulation of protein expression at the translational level, in particular as a part of stress responses, but also under normal physiological conditions (8,22,23).”
BackgroundA microRNA regulates the response of corals to thermal stress
Gajigan, A. P., & Conaco, C. (2017) · Molecular Ecology · doi:10.1111/mec.14130 · Cited by 47
Modulation of miRISC-Mediated Gene Silencing in Eukaryotes
Jungers, C. F., & Djuranović, S. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.832916 · Cited by 46
“Even though research has shown translational repression occurs first and might be one mode of controlling gene expression, it is the mRNA decay that ultimately consolidates and silences the target mRNAs (Bazzini et al., 2012; Bêthune et al., 2012; Djuranovic et al., 2011; Hu and Coller, 2012).”
The Growing Class of Novel RNAi Therapeutics
Traber, G. M., & Yu, A. (2024) · Molecular Pharmacology · doi:10.1124/molpharm.124.000895 · Cited by 51
“…can now be designed with sequences that exhibit incomplete complementary to their target mRNAs, as miRNAs are de fi ned (Yekta et al., 2004; Bazzini et al., 2012; Djuranovic et al., 2012; Jung et al., 2017; Hu et al., 2020; Hauptmann et al., 2022), yet regulate target gene expression…”
BackgroundExogenous RNA surveillance by proton-sensing TRIM25
Kim, M., Pyo, Y., Hyun, S., Jeong, M., Choi, Y., & Kim, V. N. (2025) · Science · doi:10.1126/science.ads4539 · Cited by 49
MicroRNAs and intellectual disability (ID) in Down syndrome, X-linked ID, and Fragile X syndrome
Siew, W.-H., Tan, K.-L., Babaei, M. A., Cheah, P.-S., & Ling, K. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00041 · Cited by 46
“However, a recent publication demonstrated that in the case of miR-430, the translational repression occurred independent of the deadenylation (Bazzini et al., 2012).”
BackgroundStare, T., Stare, K., Weckwerth, W., Wienkoop, S., & Gruden, K. (2017) · Proteomes · doi:10.3390/proteomes5030014 · Cited by 46
“If the translation inhibition occurs, the mRNA would still be detected even though it would not be translated to protein [44,49].”
Context-specific microRNA function in developmental complexity
Carroll, A. P., Tooney, P. A., & Cairns, M. J. (2013) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjt004 · Cited by 45
“, 2010); meanwhile, the other study identified that zebrafish miR-430 reduced the rate of translation initiation by ribosomes on target mRNA transcripts and demonstrated that reducing deadenylation did not block translational repression, suggesting that translational repression was occurring prior to complete deadenyl…”
BackgroundmicroRNAs That Promote or Inhibit Memory Formation in Drosophila melanogaster
Busto, G. U., Guven-Ozkan, T., Fulga, T. A., Vactor, D. V., & Davis, R. L. (2015) · Genetics · doi:10.1534/genetics.114.169623 · Cited by 45
“The miRNA complex, once bound, induces post-transcriptional silencing by translational repression and/or mRNA degradation (Filipowicz et al. 2008; Bazzini et al. 2012; Djuranovic et al. 2012).”
BackgroundPost-translational regulation of the maternal-to-zygotic transition
Liu, C., Ma, Y., Shang, Y., Huo, R., & Li, W. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2750-y · Cited by 47
“elegans [63, 64]; the miR-309 cluster and piRNA in Drosophila [35, 65]; miR430 in zebrafish [26, 66]; miR-18 and miR-427 in Xenopus; and miR-290 in mouse [67].”
BackgroundMicroRNAs Cause Accelerated Decay of Short-Tailed Target mRNAs
Eisen, T. J., Eichhorn, S. W., Subtelny, A. O., & Bartel, D. P. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.12.004 · Cited by 43
Human retroviral antisense mRNAs are retained in the nuclei of infected cells for viral persistence
Ma, G., Yasunaga, J., Shimura, K., Takemoto, K., Watanabe, M., Amano, M., Nakata, H., Liu, B., Zuo, X., & Matsuoka, M. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2014783118 · Cited by 44
“1D), which converts polyadenylated forms of RNA into DNA and presents them as a smear on a DNA gel (29, 30), indicated that HBZ RNA was inefficiently polyadenylated (Fig.”
BackgroundMicroRNAs, Hepatitis C Virus, and HCV/HIV-1 Co-Infection: New Insights in Pathogenesis and Therapy
Gupta, A. A., Swaminathan, G., Martín‐García, J., & Navas, S. (2012) · Viruses · doi:10.3390/v4112485 · Cited by 44
“seem to first block translation of their mRNA target and, subsequently, to mediate its degradation [8,9], although whether this is a general mechanism remains to be demonstrated.”
Zhang, X., Chen, X., Liu, Q., Zhang, S., & Hu, W. (2017) · eLife · doi:10.7554/elife.27786 · Cited by 43
“For example, certain microRNAs down-regulate the expression of their target mRNAs by first inhibiting translation and then promoting mRNA degradation (Bazzini et al., 2012; Djuranovic et al., 2012).”
BackgroundPathogenesis of idiopathic pulmonary fibrosis and its clinical implications
Spagnolo, P., Rossi, G., & Cavazza, A. (2014) · Expert Review of Clinical Immunology · doi:10.1586/1744666x.2014.917050 · Cited by 42
“In particular, the strong association of IPF with cigarette smoking and the relationship between cigarette smoke and changes in DNA methylation, posttranslational histone modifications and microRNAs (miRNAs; the most common epigenetic mechanisms) suggest that epigenetics may represent in genetically susceptible indivi…”
BackgroundMicrogenomics: Genome-Scale, Cell-Specific Monitoring of Multiple Gene Regulation Tiers
Bailey-Serres, J. N. (2013) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050312-120035 · Cited by 43
Small RNAs in Germline Development
Cook, M. S., & Blelloch, R. H. (2012) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416024-8.00006-4 · Cited by 42
Metadata
- Authors
- Bazzini, A. A., Lee, M. T., & Giraldez, A. J.
- Affiliations
- Yale University (US)
- Department of Genetics, Yale University School of Medicine, New Haven, CT 06510, USA.
- Corresponding author
- Bazzini, Ariel A.
- Lee, Miler T.
- Venue
- Science
- Published
- 2012-04-13
- Volume
- 336
- Issue
- 6078
- Pages
- 233-237
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3547538
- OpenAlex
- W2026570758
- Cited by
- 709
- References
- 30
- Citations by year
- 2026: 11 · 2025: 22 · 2024: 30 · 2023: 19 · 2022: 31 · 2021: 43 · 2020: 33 · 2019: 34 · 2018: 67 · 2017: 70 · 2016: 59 · 2015: 54 · 2014: 81 · 2013: 97 · 2012: 56
- FWCI
- 30.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (R01GM081602, R01GM102251)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (F32HD071697)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- miR-430, microRNA, protein synthesis inhibition, mRNA degradation, deadenylation, ribosome profiling, ribosome occupancy, translation initiation, Dicer, zebrafish embryos, embryonic development
- MeSH terms
- Animals, Embryo, Nonmammalian, Peptide Chain Initiation, Translational, Poly A, Ribosomes, RNA, Messenger, Protein Biosynthesis, Zebrafish, Gene Expression Regulation, Developmental, 3' Untranslated Regions, RNA Stability, Zebrafish Proteins, MicroRNAs, Ribonuclease III, Embryonic Development
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