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Database for mRNA Half-Life of 19 977 Genes Obtained by DNA Microarray Analysis of Pluripotent and Differentiating Mouse Embryonic Stem Cells
Open accessAbstract
Degradation of mRNA is one of the key processes that control the steady-state level of gene expression. However, the rate of mRNA decay for the majority of genes is not known. We successfully obtained the rate of mRNA decay for 19 977 non-redundant genes by microarray analysis of RNA samples obtained from mouse embryonic stem (ES) cells. Median estimated half-life was 7.1 h and only <100 genes, including Prdm1, Myc, Gadd45 g, Foxa2, Hes5 and Trib1, showed half-life less than 1 h. In general, mRNA species with short half-life were enriched among genes with regulatory functions (transcription factors), whereas mRNA species with long half-life were enriched among genes related to metabolism and structure (extracellular matrix, cytoskeleton). The stability of mRNAs correlated more significantly with the structural features of genes than the function of genes: mRNA stability showed the most significant positive correlation with the number of exon junctions per open reading frame length, and negative correlation with the presence of PUF-binding motifs and AU-rich elements in 3'-untranslated region (UTR) and CpG di-nucleotides in the 5'-UTR. The mRNA decay rates presented in this report are the largest data set for mammals and the first for ES cells.
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“In silico analysis showed several ARE 1 (AUUUA) and ARE 4 (12-mer A/U, max.one mismatch) sites (33) as well as a potential miR-27a/b binding site.”
From MicroRNA-27b Contributes to Lipopolysaccharide-mediated Peroxisome Proliferator-activated Receptor γ (PPARγ) mRNA Destabilization (2010) · cites this paper as [33]
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“This result is in agreement with that previously observed in mESCs 54,55 , thus suggesting the bona fide of the experiment.”
From Intragenic DNA methylation prevents spurious transcription initiation (2017) · cites this paper as [54]
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BackgroundENO1 suppresses cancer cell ferroptosis by degrading the mRNA of iron regulatory protein 1
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Post-transcriptional Regulatory Functions of Mammalian Pumilio Proteins
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“Lastly, using multiple interdependent techniques it should be mentioned that miRNA-34a has also been recently found to be significantly increased in limbic regions of the AD-affected brain, in AD monocytes and in several amyloid overexpressing transgenic murine models of AD (unpublished observations) [10,12,48,60,61,6…”
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BackgroundResultInfluentialDOMINO: Using Machine Learning to Predict Genes Associated with Dominant Disorders
Quinodoz, M., Royer‐Bertrand, B., Cisarova, K. V., Gioia, S. A. D., Superti‐Furga, A., & Rivolta, C. (2017) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2017.09.001 · Cited by 133
“, number of variants at the donor splicing site, normalized to the number of synonymous variants in the coding sequence;(20) mRNA half-life, 0 if ≤ 10 hrs or 1 if > 10 hrs.(21)”
BackgroundMassively parallel functional annotation of 3′ untranslated regions
Zhao, W., Pollack, J. L., Blagev, D. P., Zaitlen, N., McManus, M. T., & Erle, D. J. (2014) · Nature Biotechnology · doi:10.1038/nbt.2851 · Cited by 125
“In total, these segments cover >450 kb (1.5% of all annotated human 3' UTR sequence) and we used fast-UTR libraries to analyze their effects (Supplementary Note 1 and Supplementary Data 3).”
InfluentialDelmans, M., & Hemberg, M. (2016) · BMC Bioinformatics · doi:10.1186/s12859-016-0944-6 · Cited by 111
“We calculated the three derived quantities for each condition for the 2105 genes where we were able to obtain degradation rates for both cell-types [31, 32].”
MethodConnections Underlying Translation and mRNA Stability
Radhakrishnan, A., & Green, R. (2016) · Journal of Molecular Biology · doi:10.1016/j.jmb.2016.05.025 · Cited by 132
Structure of silent transcription intervals and noise characteristics of mammalian genes
Zoller, B., Nicolas, D., Molina, N., & Naef, F. (2015) · Molecular Systems Biology · doi:10.15252/msb.20156257 · Cited by 115
“Gene-specific values of f are not known but estimated between 0.01 and 0.5, based on promoter cycle times in the range of 1 – 2 h (Fig 3) and half-lives in the range of 1 – 20 h (Sharova et al , 2009), which is at least consistent with the observed difference of 0.1 – 0.2.”
InfluentialGenome-wide technology for determining RNA stability in mammalian cells
Tani, H., & Akimitsu, N. (2012) · RNA Biology · doi:10.4161/rna.22036 · Cited by 120
“Genome-wide technologies for investigating mRNA stability have revealed that the specific half-life of each mRNA is closely related to its physiological function.(22,27,34,45) Genes with shortlived mRNAs are significantly enriched among regulatory genes, which encode proteins that are required for only a limited time…”
BackgroundA DNA repair pathway can regulate transcriptional noise to promote cell fate transitions
Desai, R. V., Chen, X., Martin, B., Chaturvedi, S., Hwang, D.-W., Li, W., Chen, Y., Ding, S., Thomson, M. W., Singer, R. H., et al. (2021) · Science · doi:10.1126/science.abc6506 · Cited by 116
Timing of circadian genes in mammalian tissues
Korenčič, A., Košir, R., Bordyugov, G., Lehmann, R., Rozman, D., & Herzel, H. (2014) · Scientific Reports · doi:10.1038/srep05782 · Cited by 119
mRNA turnover rate limits siRNA and microRNA efficacy
Larsson, E., Sander, C., & Marks, D. S. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.89 · Cited by 120
“We observed a similar trend using RT–qPCR and RT–PCR measurements from 87 si/shRNAs transfected into mouse embryonic stem cells (Ren et al, 2006), confirming these results in another cell type and using an independent set of turnover rate measurements (Sharova et al, 2009) (Supplementary Figure 1).”
A hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transitionPreprint
Hsiung, C. C. ‐., Bartman, C., Huang, P., Ginart, P., Stonestrom, A. J., Keller, C. A., Face, C. J., Jahn, K. S., Evans, P., Sankaranarayanan, L., et al. (2016) · Genes & Development · doi:10.1101/gad.280859.116 · Cited by 105
“Myc and Gata2 encode for transcription factors that regulate stemness and self-renewal, and whose mature mRNA half-lives are relatively short (~15min-2h for Myc, (Dani et al. 1984; Watson 1988; Herrick and Ross 1994)~2.8h half-life for Gata2, (Sharova et al. 2009)).”
BackgroundInfluentialDelmans, M., & Hemberg, M. (2015) · doi:10.1101/020735 · Cited by 111
Treatment of neurological disorders by introducing mRNA in vivo using polyplex nanomicelles
Baba, M., Itaka, K., Kondo, K., Yamasoba, T., & Kataoka, K. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.01.017 · Cited by 109
“Although little is known about the mechanisms underlying translation control in individual cells, a few studies have reported that the half-lives of mRNA in the cytoplasm were generally in the range of hours [35-37], indicating the very transient manner of protein expression from a single mRNA molecule.”
BackgroundGalamb, O., Barták, B. K., Kalmár, A., Nagy, Z. B., Szigeti, K. A., Tulassay, Z., Igaz, P., & Molnar, B. A. (2019) · World Journal of Gastroenterology · doi:10.3748/wjg.v25.i34.5026 · Cited by 113
Pai, A. A., Cain, C. E., Mizrahi-Man, O., Leon, S. D., Lewellen, N., Veyrieras, J., Degner, J. F., Gaffney, D. J., Pickrell, J. K., Stephens, M., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003000 · Cited by 107
“Furthermore, the steadystate mRNA levels of the lowest or highest expressed genes are strongly correlated with mRNA decay rates [41,44,49,50], suggesting that in these cases, regulation of mRNA decay is likely an important determinant of gene expression levels.”
BackgroundResultGenome-wide kinetic properties of transcriptional bursting in mouse embryonic stem cells
Ochiai, H., Hayashi, T., Umeda, M., Yoshimura, M., Harada, A., Shimizu, Y., Nakano, K., Saitoh, N., Kimura, H., Liu, Z., et al. (2020) · Science Advances · doi:10.1126/sciadv.aaz6699 · Cited by 107
“The mRNA degradation rate in mESC has been genomewide analyzed (23).”
Deng, X., Berletch, J. B., Ma, W., Nguyen, D. K., Hiatt, J. B., Noble, W. S., Shendure, J., & Distèche, C. M. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.01.028 · Cited by 104
“Our results based on re-analyses of published measurements of RNA amounts following inhibition of transcription (Clark et al., 2012; Sharova et al., 2009; Tani et al., 2012) are in agreement with a longer half-life for Xlinked genes compared to autosomal genes.”
Cell‐to‐cell variability of alternative RNA splicing
Waks, Z., Klein, A. M., & Silver, P. A. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.32 · Cited by 105
“While there may be rapid fluctuations in the activity of regulatory splicing factors on the course of minutes, these would be biologically irrelevant as most mammalian mRNAs are typically stable for several hours (Yang et al, 2003; Sharova et al, 2009).”
BackgroundWang, C., Wang, H., Lieftink, C., du Chatinier, A., Gao, D., Jin, G., Jin, H., Beijersbergen, R. L., Qin, W., & Bernards, R. (2020) · Gut · doi:10.1136/gutjnl-2019-318506 · Cited by 107
Regulation of ABCA1 Protein Expression and Function in Hepatic and Pancreatic Islet Cells by miR-145
Kang, M. H., Zhang, L., Wijesekara, N., de Haan, W., Butland, S. L., Bhattacharjee, A., & Hayden, M. R. (2013) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.113.302004 · Cited by 104
“In comparison, the average length of a 3′UTR in a study of 1500 human genes was only 755 bp.(29) This suggests that multiple miRNAs regulate ABCA1.”
BackgroundWang, Y., Arribas-Layton, M., Chen, Y., Lykke‐Andersen, J., & Sen, G. L. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.08.014 · Cited by 99
Sorting and packaging of RNA into extracellular vesicles shape intracellular transcript levels
O’Grady, T. M., Njock, M., Lion, M., Bruyr, J., Mariavelle, E., Galvan, B., Boeckx, A., Struman, I., & Dequiedt, F. (2022) · BMC Biology · doi:10.1186/s12915-022-01277-4 · Cited by 101
“Interestingly, we observe that EVs are enriched for shorter mRNA and lncRNA transcripts, transcripts that are more highly spliced, and mRNA transcripts coding for ribosomal proteins; all characteristics that are associated with more stable RNA [32, 33, 57].”
BackgroundZhao, C., Zhang, H., Wong, W., Sem, X., Han, H., Ong, S., Tan, Y., Yeap, W., Gan, C. S., Ng, K.-Q., et al. (2009) · Journal of Proteome Research · doi:10.1021/pr900364p · Cited by 99
Messenger RNA Delivery for Tissue Engineering and Regenerative Medicine Applications
Patel, S., Athirasala, A., Menezes, P. D. P., Ashwanikumar, N., Zou, T., Sahay, G., & Bertassoni, L. E. (2018) · Tissue Engineering Part A · doi:10.1089/ten.tea.2017.0444 · Cited by 101
Dicer-microRNA-Myc circuit promotes transcription of hundreds of long noncoding RNAs
Zheng, G. X. Y., Do, B. T., Webster, D. E., Khavari, P. A., & Chang, H. Y. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2842 · Cited by 98
Systematic Analysis of the Determinants of Gene Expression Noise in Embryonic Stem Cells
Faure, A. J., Schmiedel, J. M., & Lehner, B. (2017) · Cell Systems · doi:10.1016/j.cels.2017.10.003 · Cited by 92
“Combining data from four independent studies(Friedel et al., 2009; Schwanhäusser et al., 2011; Sharova et al., 2009; Tippmann et al., 2012) we could validate that X-chromosome transcripts have longer half-lives than those expressed from other chromosomes (Figure 6A, Figure S19A-D).”
BackgroundFeedback Loops of the Mammalian Circadian Clock Constitute Repressilator
Pett, J. P., Korenčič, A., Wesener, F., Kramer, A., & Herzel, H. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005266 · Cited by 87
Seiler, J., Breinig, M., Caudron‐Herger, M., Polycarpou‐Schwarz, M., Boutros, M., & Diederichs, S. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx076 · Cited by 89
Coordinated control of senescence by lncRNA and a novel T-box3 co-repressor complex
Pavan Kumar, P., Emechebe, U., Smith, R. A., Franklin, S., Moore, B., Yandell, M. D., Lessnick, S. L., & Moon, A. (2014) · eLife · doi:10.7554/elife.02805 · Cited by 87
“The results we obtained were also similar to those reported for MYC mRNA (Herrick and Ross, 1994; Sharova et al., 2009), CDKN1A mRNA in HT29-tsp53 cells (Melanson et al.”
BackgroundResultInfluentialKirby, T. J., Patel, R. M., McClintock, T. S., Dupont‐Versteegden, E. E., Peterson, C. A., & McCarthy, J. J. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-08-0585 · Cited by 88
“To minimize the effect of transcript half-life on the enrichment analysis, cell type–specific transcripts were selected based on a narrow range of half-lives (Sharova et al., 2009).”
MethodBracken, C. P., Szubert, J. M., Mercer, T. R., Dinger, M. E., Thomson, D. W., Mattick, J. S., Michael, M., & Goodall, G. J. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr110 · Cited by 87
“However, the median half life reported in embryonic stem cells (26) of the 70 most represented mRNAs in the PARE library was not significantly different from the median half life of the 70 most abundant mRNAs that were not represented in the PARE library (Figure 3D).”
Leitch, A. E., Riley, N. A., Sheldrake, T. A., Festa, M., Fox, S., Duffin, R., Haslett, C., & Rossi, A. G. (2010) · European Journal of Immunology · doi:10.1002/eji.200939664 · Cited by 86
Plasma miRNA as Biomarkers for Assessment of Total-Body Radiation Exposure Dosimetry
Cui, W., Ma, J., Wang, Y., & Biswal, S. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022988 · Cited by 90
“The expression of mRNA isolated from mononuclear cells has been used to predict radiation doses; however, mRNA is intrinsically unstable [21].”
MethodA new developing class of gene delivery: messenger RNA-based therapeutics
Zhao, M., Ahern, J. O., Lyu, J., Pierucci, L., Zhou, D., & Wang, W. (2017) · Biomaterials Science · doi:10.1039/c7bm00712d · Cited by 95
Duan, J., Shi, J., Ge, X., Dölken, L., Moy, W., S, D. H. B., Shi, S., Sanders, A. R., Ross, J., & Gejman, P. V. (2013) · Scientific Reports · doi:10.1038/srep01318 · Cited by 83
Characterization of circular RNA s landscape in multiple system atrophy brain
Chen, B. J., Mills, J. D., Takenaka, K., Bliim, N., Halliday, G. M., & Janitz, M. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13752 · Cited by 84
Turner-Bridger, B., Jakobs, M. A., Mureşan, L., Wong, H. H., Franze, K., Harris, W. A., & Holt, C. E. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1806189115 · Cited by 84
“In addition, we used a consensus for the β-actin mRNA half-life of 8 h from previous publications (65, 66).”
MethodRoux, A. E., Zhang, C., Paw, J., Zavala-Solorio, J., Malahias, E., Vijay, T., Kolumam, G., Kenyon, C., & Kimmel, J. C. (2022) · Cell Systems · doi:10.1016/j.cels.2022.05.002 · Cited by 78
Dynamic lineage priming is driven via direct enhancer regulation by ERK
Hamilton, W. B., Mosesson, Y., Monteiro, R. S., Emdal, K. B., Knudsen, T. E., Francavilla, C., Barkai, N., Olsen, J. V., & Brickman, J. M. (2019) · Nature · doi:10.1038/s41586-019-1732-z · Cited by 80
Metadata
- Authors
- Sharova, L. V., Sharov, A. A., Nedorezov, T., Piao, Y., Shaik, N., & Ko, M. S. H.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Ko, M. S.H.
- Venue
- DNA Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2009-01-08
- Volume
- 16
- Issue
- 1
- Pages
- 45-58
- ISSN
- 1340-2838 (ISSN-L)
- 1756-1663
- PMC
- PMC2644350
- OpenAlex
- W2106014350
- Cited by
- 591
- References
- 57
- Citations by year
- 2026: 20 · 2025: 28 · 2024: 42 · 2023: 40 · 2022: 39 · 2021: 42 · 2020: 37 · 2019: 35 · 2018: 36 · 2017: 38 · 2016: 33 · 2015: 43 · 2014: 40 · 2013: 31 · 2012: 30
- FWCI
- 7.82
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- DNA Research (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (Z01AG000656)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Molecular Biology Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Keywords
- mRNA half-life, mRNA stability, mouse embryonic stem cells, pluripotency, cell differentiation, gene expression regulation, exon-exon junctions, AU-rich elements, 3' untranslated region, CpG, 5' untranslated region, transcription factors, steady-state mRNA levels
- MeSH terms
- Animals, Cell Differentiation, Cells, Cultured, Half-Life, Humans, Mice, Inbred C57BL, Mice, Inbred Strains, RNA, Messenger, Oligonucleotide Array Sequence Analysis, 3' Untranslated Regions, Gene Expression Profiling, RNA Stability, Databases, Genetic, Pluripotent Stem Cells, Mice, Embryonic Stem Cells
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