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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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BackgroundTranslation affects mRNA stability in a codon-dependent manner in human cells
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“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 212
“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. (2015) · Cell · doi:10.1016/j.cell.2015.09.041 · Cited by 207
“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
“…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 193
“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 204
“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
“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 199
MiRNAs: Biology, Biogenesis, their Web-based Tools, and Databases
Tafrihi, M., & Hasheminasabgorji, E. (2018) · MicroRNA · doi:10.2174/2211536607666180827111633 · Cited by 196
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 203
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 207
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 196
“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 194
“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 189
“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
“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 170
FLAM-seq: full-length mRNA sequencing reveals principles of poly(A) tail length control
Legnini, I., Alles, J., Karaiskos, N., Ayoub, S., Quedenau, C., & Rajewsky, N. (2019) · Nature Methods · doi:10.1038/s41592-019-0503-y · Cited by 187
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 171
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
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 172
“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 178
“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. J. (2017) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.07.018 · Cited by 164
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 166
The Role of microRNAs in the Pathogenesis of Herpesvirus Infection
Piedade, D., & Azevedo‐Pereira, J. M. (2016) · Viruses · doi:10.3390/v8060156 · Cited by 163
“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 164
“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
“, 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 167
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 175
“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 175
“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
“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 159
“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 156
“…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
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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