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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Global measurements indicate that miRNA targeting causes mostly mRNA destabilization, with translational repression comprising a detectable but minor component of overall repression.
“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]
The only known exception to the pattern of miRNA targeting causing mostly mRNA destabilization is the transient translational repression observed in early zebrafish embryos.
“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]
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 destabilization.
“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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“To analyze the poly(A) tail status 876 Molecular Cell 61, 874–885, March 17, 2016 ª2016 Elsevier Inc. of maternal mRNAs, we utilized poly(G/I) tailing-based PAT assay (Kusov et al., 2001), which can accurately recapitulate the changes of poly(A) tail lengths (Figures S2A–S2C) (Bazzini et al., 2012).”
microRNAs Biogenesis, Functions and Role in Tumor Angiogenesis
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Ribosome Profiling: Global Views of TranslationPreprint
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“Later work in developing zebrafish embryos showed that strong translational repression precedes mRNA decay during the activation of miR-430 in the maternal-to-zygotic transition (Bazzini et al. 2012).”
BackgroundTranslation affects mRNA stability in a codon-dependent manner in human cells
Wu, Q., Medina, S. G., Kushawah, G., DeVore, M. L., Castellano, L. A., Hand, J. M., Wright, M., & Bazzini, A. A. (2019) · eLife · doi:10.7554/elife.45396 · Cited by 283 · see citing works
Self-citationFrom guide to target: molecular insights into eukaryotic RNA-interference machinery
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Ribosome profiling reveals resemblance between long non-coding RNAs and 5′ leaders of coding RNAs
Chew, G.-L., Pauli, A., Rinn, J. L., Regev, A., Schier, A. F., & Valen, E. (2013) · Development · doi:10.1242/dev.098343 · Cited by 275 · see citing works
“Our dataset increases the depth of previous ribosome profiling datasets in zebrafish by an order of magnitude (Bazzini et al., 2012) D E V E L O P M E N T identification of potential protein isoforms, furthering ongoing efforts to refine zebrafish genome annotation (Kettleborough et al., 2013).”
MethodMicroRNAs shape the neuronal landscape
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microRNA target prediction programs predict many false positivesPreprint
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“the abundance of target mRNAs is a good approximation of the effect of the miRNA on protein abundance, at least at steady-state in vertebrates (Hendrickson et al. 2009; Guo et al. 2010; Bazzini et al. 2012), and transcriptomic methods are more sensitive than prote-”
MethodPhase Transitions in the Assembly and Function of Human miRISC
Sheu‐Gruttadauria, J., & MacRae, I. J. (2018) · Cell · doi:10.1016/j.cell.2018.02.051 · Cited by 258 · see citing works
“Silencing includes elements of both translational repression and mRNA decay (Bagga et al., 2005; Bazzini et al., 2012; Djuranovic et al., 2012; Guo et al., 2010).”
Standardized annotation of translated open reading frames
Mudge, J. M., Ruiz‐Orera, J., Prensner, J. R., Brunet, M. A., Calvet, F., Jungreis, I., González, J. M., Magrane, M., Martinez, T. F., Schulz, J. F., et al. (2022) · Nature Biotechnology · doi:10.1038/s41587-022-01369-0 · Cited by 251 · see citing works
Self-citationGWIPS-viz: development of a ribo-seq genome browser
Michel, A. M., Fox, G., Kiran, A. M., Bo, C. D., O’Connor, P. B. F., Heaphy, S. M., Mullan, J. P. A., Donohue, C. A., Higgins, D. G., & Baranov, P. V. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1035 · Cited by 249 · see citing works
“Since the original publication, the technique has been carried out in many organisms including Homo sapiens (3–11) Mus musculus (3,7,9,12,13) Danio rerio (14), Caenorhabditis elegans (4,15), S.”
MethodNucleo-cytosolic Shuttling of ARGONAUTE1 Prompts a Revised Model of the Plant MicroRNA Pathway
Bologna, N. G., Iselin, R., Abriata, L. A., Sarazin, A., Pumplin, N., Jay, F., Grentzinger, T., Peraro, M. D., & Voinnet, O. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.01.007 · Cited by 249 · see citing works
Selective autophagy degrades DICER and AGO2 and regulates miRNA activity
Gibbings, D., Mostowy, S., Jay, F., Schwab, Y., Cossart, P., & Voinnet, O. (2012) · Nature Cell Biology · doi:10.1038/ncb2611 · Cited by 249 · see citing works
miRNA sponges: soaking up miRNAs for regulation of gene expression
Bak, R. O., & Mikkelsen, J. G. (2013) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1213 · Cited by 239 · see citing works
Genome-wide assessment of differential translations with ribosome profiling data
Xiao, Z., Zou, Q., Liu, Y., & Yang, X. (2016) · Nature Communications · doi:10.1038/ncomms11194 · Cited by 236 · see citing works
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“…repression are increasingly recognized as being rather similar in plants and animals; in both cases, targets are typically repressed by a combination of mRNA degradation and translational repression (Brodersen et al., 2008; Guo et al., 2010; Bazzini et al., 2012; S. Li et al., 2013).”
BackgroundPABP Cooperates with the CCR4-NOT Complex to Promote mRNA Deadenylation and Block Precocious Decay
Yi, H., Park, J., Ha, M., Lim, J., Chang, H., & Kim, V. N. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.05.009 · Cited by 226 · see citing works
microRNA strand selection: Unwinding the rules
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Transcriptome-wide Discovery of microRNA Binding Sites in Human Brain
Boudreau, R. L., Jiang, P., Gilmore, B. L., Spengler, R. M., Tirabassi, R. S., Nelson, J. A., Ross, C. A., Xing, Y., & Davidson, B. L. (2014) · Neuron · doi:10.1016/j.neuron.2013.10.062 · Cited by 217 · see citing works
Insect MicroRNAs: Biogenesis, expression profiling and biological functions
Lucas, K. J., & Raikhel, A. S. (2012) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2012.10.009 · Cited by 203 · see citing works
“Ribosome profiling experiments with temporal resolution and poly(A) tail analysis in Zebrafish indicate that miR-430 works to induce translational repression by reducing the rate of translation initiation, followed by mRNA decay through deadenylation (Bazzini et al., 2012).”
BackgroundKinetic analysis reveals successive steps leading to miRNA‐mediated silencing in mammalian cells
Béthune, J., Artus-Revel, C. G., & Filipowicz, W. (2012) · EMBO Reports · doi:10.1038/embor.2012.82 · Cited by 201 · see citing works
“During revision of our manuscript, two papers reported that also in zebrafish and Drosophila S2 cells, translational repression precedes mRNA deadenylation and decay [29,30].”
Pausing on Polyribosomes: Make Way for Elongation in Translational Control
Richter, J. D., & Coller, J. M. (2015) · Cell · doi:10.1016/j.cell.2015.09.041 · Cited by 204 · see citing works
“Although ribosome profiles derived from developing zebrafish embryos showed that at least miR-430 did not induce ribosome drop off (Bazzini et al., 2012), it remains an open question as to the extent to which miRNAs can promote post-initiation mRNA silencing.”
Brain, O., Owens, B. M. J., Pichulik, T., Allan, P., Khatamzas, E., Leslie, A. J., Steevels, T. A. M., Sharma, S., Mayer, A., Catuneanu, A., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.035 · Cited by 201 · see citing works
“…MDP treatment of DCs, and requires RIPK-2 to exert this effect. miR-29 Regulates the Expression of Multiple Inflammatory Genes in DCs Including IL12B miRNAs act by translational inhibition, followed by deadenylation and decay of their target mRNA (Djuranovic et al., 2012; Bazzini et al., 2012).”
BackgroundExtensive Oscillatory Gene Expression during C. elegans Larval Development
Hendriks, G., Gaidatzis, D., Aeschimann, F., & Großhans, H. (2014) · Molecular Cell · doi:10.1016/j.molcel.2013.12.013 · Cited by 199 · see citing works
“Ribosome profiling We adapted published protocols (Ingolia et al., 2012; Bazzini et al., 2012) to perform ribosome profiling.”
Narasimhan, M., Patel, D., Vedpathak, D., Rathinam, M., Henderson, G. I., & Mahimainathan, L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051111 · Cited by 201 · see citing works
“Though, several studies show miRNA induced protein repression strongly correlates to mRNA levels [53,55,56], the possibility of miRs inducing translational repression even before mRNA deadenylation and decay have been very recently reported [52,57].”
BackgroundBartoszewski, R., Moszyńska, A., Serocki, M., Cabaj, A., Polten, A., Ochocka, R., Dell'Italia, L., Bartoszewska, S., Króliczewski, J., Dąbrowski, M., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201802650rr · Cited by 199 · see citing works
“miRNA activity is repressing gene activity by blocking translation of their mRNA targets (52, 53) or by promoting”
BackgroundXiong, Z., Xu, K., Lin, Z., Kong, F., Wang, Q., Quan, Y., Sha, Q., Li, F., Zou, Z., Liu, L., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00928-6 · Cited by 195 · see citing works
MiRNAs: Biology, Biogenesis, their Web-based Tools, and Databases
Tafrihi, M., & Hasheminasabgorji, E. (2018) · MicroRNA · doi:10.2174/2211536607666180827111633 · Cited by 196 · see citing works
Schopp, I. M., Ramirez, C. C. A., Debeljak, J., Kreibich, E., Skribbe, M., Wild, K., & Béthune, J. (2017) · Nature Communications · doi:10.1038/ncomms15690 · Cited by 189 · see citing works
Transfection of microRNA Mimics Should Be Used with Caution
Jin, H. Y., González-Martín, A., Miletic, A. V., Lai, M., Knight, S., Sabouri-Ghomi, M., Head, S. R., Macauley, M. S., Rickert, R. C., & Xiao, C. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00340 · Cited by 194 · see citing works
Principles of miRNA–mRNA interactions: beyond sequence complementarity
Afonso-Grunz, F., & Müller, S. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1922-2 · Cited by 193 · see citing works
“decay [12–14].”
Translational Landscape of Photomorphogenic Arabidopsis
Liu, M., Wu, S.-H., Wu, J.-F., Lin, W., Wu, Y., Tsai, T.-Y., Tsai, H.-L., & Wu, S. (2013) · The Plant Cell · doi:10.1105/tpc.113.114769 · Cited by 188 · see citing works
“MiRNAs were found to act first on mRNA translation, then decapping or decay of mRNAs (Bazzini et al., 2012; Djuranovic et al., 2012).”
BackgroundmicroRNAs in the Same Clusters Evolve to Coordinately Regulate Functionally Related Genes
Wang, Y., Luo, J., Zhang, H., & Lü, J. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw089 · Cited by 187 · see citing works
“An intriguing observation is the miR-430 cluster in zebrafish, which plays important roles in maternal mRNA clearance and translational regulation during development (Giraldez et al. 2006; Bartel 2009; Bazzini et al. 2012).”
MicroRNA-9 Modulates Hes1 Ultradian Oscillations by Forming a Double-Negative Feedback Loop
Bonev, B., Stanley, P., & Papalopulu, N. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.05.017 · Cited by 186 · see citing works
“In fact, recent evidence suggests that both mechanisms may occur on the same targets (Bazzini et al., 2012).”
BackgroundBrümmer, A., & Hausser, J. (2014) · BioEssays · doi:10.1002/bies.201300104 · Cited by 185 · see citing works
FLAM-seq: full-length mRNA sequencing reveals principles of poly(A) tail length control
Legnini, I., Alles, J., Karaiskos, N., Ayoub, S., Rajewsky, N., & Rajewsky, N. (2019) · Nature Methods · doi:10.1038/s41592-019-0503-y · Cited by 180 · see citing works
mTAIL-seq reveals dynamic poly(A) tail regulation in oocyte-to-embryo developmentPreprint
Lim, J., Lee, M., Son, A., Chang, H., & Kim, V. N. (2016) · Genes & Development · doi:10.1101/gad.284802.116 · Cited by 172 · see citing works
Self-citationBidirectional processing of pri-miRNAs with branched terminal loops by Arabidopsis Dicer-like1
Zhu, H., Zhou, Y., Castillo-González, C., Lu, A., Ge, C., Zhao, Y.-T., Duan, L., Li, Z., Axtell, M. J., Wang, X. J., et al. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2646 · Cited by 167 · see citing works
miRNA–transcription factor interactions: a combinatorial regulation of gene expression
Arora, S., Rana, R., Chhabra, A., Jaiswal, A., & Rani, V. (2013) · Molecular Genetics and Genomics · doi:10.1007/s00438-013-0734-z · Cited by 166 · see citing works
“Further, action of miRNA-430 in zebrafish embryos occurs through reduction in ribosome density on the target mRNA, decreasing the rate of initiation of translation followed by deadenylation and hence translational repression (Bazzini et al. 2012).”
BackgroundPoly(A)-Specific Ribonuclease Mediates 3′-End Trimming of Argonaute2-Cleaved Precursor MicroRNAs
Yoda, M., Cifuentes, D., Izumi, N., Sakaguchi, Y., Suzuki, T., Giráldez, A. J., & Tomari, Y. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.09.029 · Cited by 165 · see citing works
“set of 881 nontarget genes is defined as in Bazzini et al. (2012). Briefly, it consists only of genes with 30 UTRs R300 nt and mismatches of R6 nt to the miR-430 seed in either the CDS or the 30 UTR.”
Structural Foundations of RNA Silencing by Argonaute
Sheu-Gruttadauria, J., & MacRae, I. (2017) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.07.018 · Cited by 157 · see citing works
MicroRNAs , transforming growth factor beta‐1, and tissue fibrosis
Bowen, T., Jenkins, R. L., & Fraser, D. J. (2012) · The Journal of Pathology · doi:10.1002/path.4119 · Cited by 162 · see citing works
The Role of microRNAs in the Pathogenesis of Herpesvirus Infection
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“The most recent studies suggest that these two mechanisms occur in sequence [52–56], indicating that destabilization of target mRNA is the last and predominant step in mRNA repression [52,57].”
BackgroundHorman, S. R., Janas, M. M., Litterst, C. M., Wang, B., MacRae, I. J., Sever, M. J., Morrissey, D. V., Graves, P. R., Luo, B., Umesalma, S., et al. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.03.015 · Cited by 161 · see citing works
“However, the majority of mammalian miRNAs are imperfectly complementary to their mRNA targets, and thus mediate translational repression and mRNA destabilization (Janas and Novina, 2012; Bazzini et al., 2012; Djuranovic et al., 2012; Guo et al., 2010).”
BackgroundHigh-Throughput Analysis Reveals Rules for Target RNA Binding and Cleavage by AGO2
Becker, W. R., Ober-Reynolds, B., Jouravleva, K., Jolly, S. M., Zamore, P. D., & Greenleaf, W. J. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.06.012 · Cited by 161 · see citing works
“, 2010) or inhibit mRNA translation (Doench et al., 2003; Doench and Sharp, 2004; Hendrickson et al., 2009; Bazzini et al., 2012).”
Specificity factors in cytoplasmic polyadenylation
Charlesworth, A. G., Meijer, H. A., & de Moor, C. H. (2013) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1171 · Cited by 160 · see citing works
The intricate balance between microRNA‐induced mRNA decay and translational repression
Naeli, P., Winter, T., Hackett, A. P., Alboushi, L., & Jafarnejad, S. M. (2022) · FEBS Journal · doi:10.1111/febs.16422 · Cited by 160 · see citing works
“While high-throughput analyses have shown that the bulk of miRNA-induced repression is due to mRNA decay [127, 128], temporal dissections have demonstrated that there is translational inhibition of various degrees preceding mRNA deadenylation [8-10, 127, 129-131] and that miRNA-induced decay can only occur after this…”
BackgroundEpigenetics in teleost fish: From molecular mechanisms to physiological phenotypes
Best, C., Ikert, H., Kostyniuk, D. J., Craig, P. M., Navarro‐Martín, L., Marandel, L., & Mennigen, J. A. (2018) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2018.01.006 · Cited by 165 · see citing works
“mRNA translation and/or protein abundance has been identified in developing zebrafish (Bazzini et al., 2005) and adult rainbow trout (Mennigen et al.”
BackgroundKarginov, F. V., & Hannon, G. J. (2013) · Genes & Development · doi:10.1101/gad.215939.113 · Cited by 156 · see citing works
“2010), experiments with kinetic resolution have shown that the effect of Ago proteins on translational repression may be important during transitions between cellular states (Bazzini et al. 2012; Bethune et al. 2012; Djuranovic et al. 2012).”
BackgroundFunctional Importance of Dicer Protein in the Adaptive Cellular Response to Hypoxia
Ho, J. J. D., Metcalf, J. L., Yan, M. S., Turgeon, P. J., Wang, J. J., Chalsev, M., Petruzziello-Pellegrini, T. N., Tsui, A. K. Y., He, J. Z., Dhamko, H., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.373365 · Cited by 156 · see citing works
“Importantly, two recent independent studies that examined the kinetics of microRNA-mediated translational inhibition and mRNA degradation have found that mRNA degradation follows translational inhibition (31, 32).”
BackgroundMechanistic Insights into MicroRNA-Mediated Gene SilencingPreprint
Duchaîne, T. F., & Fabian, M. R. (2018) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a032771 · Cited by 146 · see citing works
“…inhibition can be observed before detectable mRNA deadenylation (Fabian et al. 2009; Zdanowicz et al. 2009). miRNA-mediated translational repression before mRNA deadenylation was also reported in cells (Bethune et al. 2012; Djuranovic et al. 2012) and zebrafish embryos (Bazzini et al. 2012).”
Background
- 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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