Functional 5′ UTR mRNA structures in eukaryotic translation regulation and how to find them
Open accessAbstract
RNA molecules can fold into intricate shapes that can provide an additional layer of control of gene expression beyond that of their sequence. In this Review, we discuss the current mechanistic understanding of structures in 5' untranslated regions (UTRs) of eukaryotic mRNAs and the emerging methodologies used to explore them. These structures may regulate cap-dependent translation initiation through helicase-mediated remodelling of RNA structures and higher-order RNA interactions, as well as cap-independent translation initiation through internal ribosome entry sites (IRESs), mRNA modifications and other specialized translation pathways. We discuss known 5' UTR RNA structures and how new structure probing technologies coupled with prospective validation, particularly compensatory mutagenesis, are likely to identify classes of structured RNA elements that shape post-transcriptional control of gene expression and the development of multicellular organisms.
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
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?
Only 13% of human 5′ UTRs are shorter than 50 nt and thus covered by Optimus 5-Prime.
“Because only 13% of human 5′ UTRs are shorter than 50 nt and thus covered by Optimus 5-Prime, we next asked whether the approach introduced here could be extended to longer 5′ UTRs.”
From Human 5′ UTR design and variant effect prediction from a massively parallel translation assay (2019) · cites this paper as [45]
The section ‘5′ UTRs as platforms for RNA structure’ (page unavailable) reports a median human 5′ UTR length of 218 nucleotides, supporting the general point that many are longer than 50 nt. It does not give the 13% figure or discuss which UTRs Optimus 5-Prime covers. (LLM, conf=0.84)
Experimental — accuracy not yet measuredHuman 5′ UTR sequences vary in length from tens to thousands of nucleotides with a median length of 218 nt.
“Human 5′ UTR sequences vary in length from tens to thousands of nucleotides with a median length of 218 nt44,45.”
From Human 5′ UTR design and variant effect prediction from a massively parallel translation assay (2019) · cites this paper as [45]
Higher GC content and highly negative folding minimal free energy (ΔG) of 5′UTRs correlate with inhibition of translation.
“In addition to greater length, the TPL sequence has a higher GC content and highly negative folding minimal free energy (ΔG), which correlates with inhibition of translation [4,7,45,46] (Table 1).”
From Effects of Combinations of Untranslated-Region Sequences on Translation of mRNA (2023) · cites this paper as [4]
Untranslated regions harbor regulatory elements that influence translational efficiency and mRNA stability within cells.
“The untranslated regions harbor regulatory elements that influence translational efficiency and mRNA stability within cells [10,11].”
From Identification of novel 5’ UTR variants for enhanced mRNA translation and vaccine immunogenicity (2026) · cites this paper as [10]
Shorter 5′UTRs are better for mRNA translation.
“(iii) Shorter 5′UTRs may be used, as past research has indicated that this type of 5′UTR is better for mRNA translation (Leppek et al. 2018).”
From Modifications of mRNA vaccine structural elements for improving mRNA stability and translation efficiency (2022) · cites this paper as Leppek et al. 2018
The section ‘5′ UTRs as platforms for RNA structure’ describes variation in UTR length but does not compare translation efficiency by length. ‘5′ UTR structures in ribosome scanning’ notes that some exceptionally short UTRs permit scanning-free initiation; it does not say shorter UTRs are generally better for translation. Searches for short UTRs and translational efficiency found no such comparison in our copy. (LLM, conf=0.70)
Experimental — accuracy not yet measured
The 5′ UTR is mainly involved in translation of its downstream ORF sequence, and the Kozak sequence is generally added after the 5′ UTR sequence to improve translation efficiency.
“The 5′ UTR is mainly involved in translation of its downstream ORF sequence.132,133 The Kozak sequence is generally added after the 5′ UTR sequence to improve translation efficiency.134”
From Advances in COVID-19 mRNA vaccine development (2022) · cites this paper as [133]
Engineered UTR sequences minimize regions that prevent ribosomes from scanning the mRNA transcript, such as sequences with secondary and tertiary structure in the 5′ UTR.
“Furthermore, they minimize regions that prevent ribosomes from scanning the mRNA transcript, such as sequences with secondary and tertiary structure (for example, hairpins) in the 5′ UTR20.”
From mRNA vaccines for infectious diseases: principles, delivery and clinical translation (2021) · cites this paper as [20]
Sequences of 5′ and 3′ untranslated regions (UTRs) play a key role in the stability of mRNA molecules and in their translational efficiency.
“Sequences of 5′ and 3′ untranslated regions (UTRs) are responsible for translational efficiency and stability of mRNA.”
From Effects of Combinations of Untranslated-Region Sequences on Translation of mRNA (2023) · cites this paper as [4]
RNA secondary structure elements can facilitate higher-order interactions that promote assembly of intermolecular complexes involving RBPs and regulatory RNA molecules, making overall impact of secondary structure multifaceted.
“However, RNA secondary structure elements can also facilitate higher-order interactions that promote the assembly of intermolecular complexes involving RBPs and regulatory RNA molecules [10], making the overall impact of secondary structure multifaceted.”
From Identification of novel 5’ UTR variants for enhanced mRNA translation and vaccine immunogenicity (2026) · cites this paper as [10]
An extensively stable secondary structure with high GC content in the 5′ UTR, particularly in the 5′-proximal region, tends to decrease translation efficiency.
“It is well established that an extensively stable secondary structure with high GC content in the 5′ UTR -particularly in the 5′-proximal region -tends to decrease translation efficiency [10,34].”
From Identification of novel 5’ UTR variants for enhanced mRNA translation and vaccine immunogenicity (2026) · cites this paper as [10]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Belew, A. T., Meškauskas, A., Musalgaonkar, S., Advani, V. M., Sulima, S. O., Kasprzak, W. K., Shapiro, B. A., & Dinman, J. D. (2014) · Nature · doi:10.1038/nature13429 · Cited by 149 · see citing works
RetractedMfold web server for nucleic acid folding and hybridization prediction
Zuker, M. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg595 · Cited by 13,404 · see citing works
Lorenz, R., Bernhart, S. H., Höner zu Siederdissen, C., Tafer, H., Flamm, C., Stadler, P. F., & Hofacker, I. L. (2011) · Algorithms for Molecular Biology · doi:10.1186/1748-7188-6-26 · Cited by 5,098 · see citing works
Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq
Dominissini, D., Moshitch-Moshkovitz, S., Schwartz, S., Salmon-Divon, M., Ungar, L., Osenberg, S., Cesarkas, K., Jacob-Hirsch, J., Amariglio, N., Kupiec, M., et al. (2012) · Nature · doi:10.1038/nature11112 · Cited by 4,884 · see citing works
Kozak, M. (1986) · Cell · doi:10.1016/0092-8674(86)90762-2 · Cited by 4,741 · see citing works
N6-methyladenosine-dependent regulation of messenger RNA stability
Wang, X., Lu, Z., Gomez, A., Hon, G. C., Yue, Y., Han, D., Fu, Y., Parisien, M., Dai, Q., Jia, G., et al. (2014) · Nature · doi:10.1038/nature12730 · Cited by 4,558 · see citing works
N6-methyladenosine Modulates Messenger RNA Translation Efficiency
Wang, X., Zhao, B. S., Roundtree, I. A., Lu, Z., Han, D., Ma, H., Weng, X., Chen, K., Shi, H., & He, C. (2015) · Cell · doi:10.1016/j.cell.2015.05.014 · Cited by 3,483 · see citing works
Regulation of Translation Initiation in Eukaryotes: Mechanisms and Biological Targets
Sonenberg, N., & Hinnebusch, A. G. (2009) · Cell · doi:10.1016/j.cell.2009.01.042 · Cited by 3,304 · see citing works
The mechanism of eukaryotic translation initiation and principles of its regulation
Jackson, R. J., Hellen, C. U. T., & Pestova, T. V. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2838 · Cited by 2,759 · see citing works
The Transcriptional Landscape of the Yeast Genome Defined by RNA Sequencing
Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M., & Snyder, M. (2008) · Science · doi:10.1126/science.1158441 · Cited by 2,479 · see citing works
Post-transcriptional gene regulation by mRNA modifications
Zhao, B. S., Roundtree, I. A., & He, C. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.132 · Cited by 2,418 · see citing works
Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis
Legnini, I., Di Timoteo, G., Rossi, F., Morlando, M., Briganti, F., Sthandier, O., Fatica, A., Santini, T., Andronache, A., Wade, M., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.02.017 · Cited by 2,173 · see citing works
FMRP Stalls Ribosomal Translocation on mRNAs Linked to Synaptic Function and Autism
Darnell, J. C., Van Driesche, S. J., Zhang, C., Hung, K. Y. S., Mele, A., Fraser, C. E., Stone, E. F., Chen, C., Fak, J. J., Chi, S. W., et al. (2011) · Cell · doi:10.1016/j.cell.2011.06.013 · Cited by 2,072 · see citing works
N6-methyladenosine-dependent RNA structural switches regulate RNA–protein interactions
Liu, N., Dai, Q., Zheng, G., He, C., Parisien, M., & Pan, T. (2015) · Nature · doi:10.1038/nature14234 · Cited by 1,988 · see citing works
5′ UTR m6A Promotes Cap-Independent Translation
Meyer, K. D., Patil, D. P., Zhou, J. L., Zinoviev, A., Skabkin, M. A., Elemento, O., Pestova, T. V., Qian, S., & Jaffrey, S. R. (2015) · Cell · doi:10.1016/j.cell.2015.10.012 · Cited by 1,812 · see citing works
Pamudurti, N. R., Bartok, O., Jens, M., Ashwal-Fluss, R., Stottmeister, C., Ruhe, L., Hanan, M., Wyler, E., Perez-Hernandez, D., Ramberger, E., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.02.021 · Cited by 1,810 · see citing works
The m(6)A Methyltransferase METTL3 Promotes Translation in Human Cancer Cells
Lin, S., Choe, J., Du, P., Triboulet, R., & Gregory, R. I. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.03.021 · Cited by 1,531 · see citing works
A compendium of RNA-binding motifs for decoding gene regulation
Ray, D., Kazan, H., Cook, K. B., Weirauch, M. T., Najafabadi, H. S., Li, X., Gueroussov, S., Albu, M., Zheng, H., Yang, A., et al. (2013) · Nature · doi:10.1038/nature12311 · Cited by 1,480 · see citing works
Messenger-RNA-binding proteins and the messages they carry
Dreyfuss, G., Kim, V. N., & Kataoka, N. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm760 · Cited by 1,469 · see citing works
Morris, K. V., & Mattick, J. S. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3722 · Cited by 1,389 · see citing works
Translational control in stress and apoptosis
Holčı́k, M., & Sonenberg, N. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1618 · Cited by 1,366 · see citing works
A Red carpet for iron metabolism
Muckenthaler, M. U., Rivella, S., Hentze, M. W., & Galy, B. (2017) · Cell · doi:10.1016/j.cell.2016.12.034 · Cited by 1,319 · see citing works
Dynamic m6A mRNA methylation directs translational control of heat shock response
Zhou, J. L., Wan, J., Gao, X., Zhang, X., Jaffrey, S. R., & Qian, S. (2015) · Nature · doi:10.1038/nature15377 · Cited by 1,226 · see citing works
Translational control by 5′-untranslated regions of eukaryotic mRNAs
Hinnebusch, A. G., Ivanov, I. P., & Sonenberg, N. (2016) · Science · doi:10.1126/science.aad9868 · Cited by 1,079 · see citing works
The dynamic N1-methyladenosine methylome in eukaryotic messenger RNA
Dominissini, D., Nachtergaele, S., Moshitch-Moshkovitz, S., Peer, E., Kol, N., Ben-Haim, M. S., Dai, Q., Segni, A. D., Salmon‐Divon, M., Clark, W. C., et al. (2016) · Nature · doi:10.1038/nature16998 · Cited by 1,026 · see citing works
Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat
Carrieri, C., Cimatti, L., Biagioli, M., Beugnet, A., Zucchelli, S., Fedele, S., Pesce, E., Ferrer, I., Collavin, L., Santoro, C., et al. (2012) · Nature · doi:10.1038/nature11508 · Cited by 1,001 · see citing works
Untranslated regions of mRNAs.
(2002) · Genome biology · doi:10.1186/gb-2002-3-3-reviews0004 · Cited by 987 · see citing works
Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function
Darnell, J. C., Jensen, K. B., Jin, P., Brown, V., Warren, S. T., & Darnell, R. B. (2001) · Cell · doi:10.1016/s0092-8674(01)00566-9 · Cited by 952 · see citing works
Calvo, S. E., Pagliarini, D. J., & Mootha, V. K. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810916106 · Cited by 914 · see citing works
DNA G-quadruplexes in the human genome: detection, functions and therapeutic potential
Hänsel‐Hertsch, R., Antonio, M. D., & Balasubramanian, S. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.3 · Cited by 882 · see citing works
Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo
Rouskin, S., Zubradt, M. M., Stefan Washietl, A., Kellis, M., & Weissman, J. S. (2013) · Nature · doi:10.1038/nature12894 · Cited by 860 · see citing works
An RNA G-quadruplex in the 5′ UTR of the NRAS proto-oncogene modulates translation
Kumari, S., Bugaut, A., Huppert, J. L., & Balasubramanian, S. (2007) · Nature Chemical Biology · doi:10.1038/nchembio864 · Cited by 822 · see citing works
A majority of m6A residues are in the last exons, allowing the potential for 3′ UTR regulationPreprint
Ke, S., Alemu, E. A., Mertens, C., Gantman, E. C., Fak, J. J., Mele, A., Haripal, B., Zucker-Scharff, I., Moore, M. J., Park, C. Y., et al. (2015) · Genes & Development · doi:10.1101/gad.269415.115 · Cited by 815 · see citing works
Genetic Control by a Metabolite Binding mRNA
Nahvi, A., Sudarsan, N., Ebert, M. S., Zou, X., Brown, K. L., & Breaker, R. R. (2002) · Chemistry & Biology · doi:10.1016/s1074-5521(02)00224-7 · Cited by 802 · see citing works
The Scanning Mechanism of Eukaryotic Translation Initiation
Hinnebusch, A. G. (2014) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060713-035802 · Cited by 798 · see citing works
In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features
Ding, Y., Tang, Y., Kwok, C. K., Zhang, Y., Bevilacqua, P. C., & Assmann, S. M. (2014) · Nature · doi:10.1038/nature12756 · Cited by 775 · see citing works
Genome-wide measurement of RNA secondary structure in yeast
Kertesz, M., Wan, Y., Mazor, E., Rinn, J. L., Nutter, R. C., Chang, H. Y., & Segal, E. (2010) · Nature · doi:10.1038/nature09322 · Cited by 765 · see citing works
Structural imprints in vivo decode RNA regulatory mechanisms
Spitale, R. C., Flynn, R. A., Zhang, Q. C., Crisalli, P., Lee, B., Jung, J., Kuchelmeister, H. Y., Batista, P. J., Torre, E. A., Kool, E. T., et al. (2015) · Nature · doi:10.1038/nature14263 · Cited by 745 · see citing works
Molecular mechanisms of translation initiation in eukaryotes
Pestova, T. V., KOLUPAEVA, V. G., Lomakin, I. B., Pilipenko, E. V., Shatsky, I. N., Agol, V. I., & Hellen, C. U. T. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111145798 · Cited by 742 · see citing works
Influences of mRNA secondary structure on initiation by eukaryotic ribosomes.
Kozak, M. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.9.2850 · Cited by 687 · see citing works
Riboswitches and the RNA WorldPreprint
Breaker, R. R. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a003566 · Cited by 679 · see citing works
Brierley, I., Digard, P., & Inglis, S. C. (1989) · Cell · doi:10.1016/0092-8674(89)90124-4 · Cited by 669 · see citing works
RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP)
Siegfried, N. A., Busan, S., Rice, G. M., Nelson, J. A. E., & Weeks, K. M. (2014) · Nature Methods · doi:10.1038/nmeth.3029 · Cited by 662 · see citing works
5'-UTR RNA G-quadruplexes: translation regulation and targeting
Bugaut, A., & Balasubramanian, S. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks068 · Cited by 643 · see citing works
Heterogeneous Ribosomes Preferentially Translate Distinct Subpools of mRNAs Genome-wide
Shi, Z., Fujii, K., Kovary, K. M., Genuth, N. R., Röst, H. L., Teruel, M. N., & Barna, M. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.05.021 · Cited by 638 · see citing works
Self-citationRNA G-quadruplexes cause eIF4A-dependent oncogene translation in cancer
Wolfe, A. L., Singh, K., Zhong, Y., Drewe, P., Rajasekhar, V. K., Sanghvi, V. R., Mavrakis, K. J., Jiang, M., Roderick, J. E., Van der Meulen, J., et al. (2014) · Nature · doi:10.1038/nature13485 · Cited by 635 · see citing works
Posttranscriptional Gene Regulation by Long Noncoding RNA
Yoon, J., Abdelmohsen, K., & Gorospe, M. (2012) · Journal of Molecular Biology · doi:10.1016/j.jmb.2012.11.024 · Cited by 628 · see citing works
Schwartz, S., Agarwala, S. D., Mumbach, M. R., Jovanović, M., Mertins, P., Shishkin, A., Tabach, Y., Mikkelsen, T. S., Satija, R., Ruvkun, G., et al. (2013) · Cell · doi:10.1016/j.cell.2013.10.047 · Cited by 627 · see citing works
Pelletier, J., & Sonenberg, N. (1985) · Cell · doi:10.1016/0092-8674(85)90200-4 · Cited by 610 · see citing works
Regulation by 3′-Untranslated Regions
Mayr, C. (2017) · Annual Review of Genetics · doi:10.1146/annurev-genet-120116-024704 · Cited by 588 · see citing works
Ribosome-Mediated Specificity in Hox mRNA Translation and Vertebrate Tissue Patterning
Kondrashov, N., Pusic, A. D., Stumpf, C. R., Shimizu, K., Hsieh, A. C., Xue, S., Ishijima, J., Shiroishi, T., & Barna, M. (2011) · Cell · doi:10.1016/j.cell.2011.03.028 · Cited by 581 · see citing works
Self-citationHentze, M. W., Caughman, S. W., Rouault, T. A., Barriocanal, J. G., Dancis, A., Harford, J. B., & Klausner, R. D. (1987) · Science · doi:10.1126/science.3685996 · Cited by 571 · see citing works
Internal initiation of translation mediated by the 5′ leader of a cellular mRNA
Macejak, D. G., & Sarnow, P. (1991) · Nature · doi:10.1038/353090a0 · Cited by 563 · see citing works
Visualizing the molecular sociology at the HeLa cell nuclear periphery
Mahamid, J., Pfeffer, S., Schaffer, M., Villa, E., Danev, R., Cuellar, L. K., Förster, F. G., Hyman, A. A., Plitzko, J. M., & Baumeister, W. P. (2016) · Science · doi:10.1126/science.aad8857 · Cited by 561 · see citing works
Identification and Classification of Conserved RNA Secondary Structures in the Human Genome
Pedersen, J. S., Bejerano, G., Siepel, A. C., Rosenbloom, K. R., Lindblad‐Toh, K., Lander, E. S., Kent, J., Miller, W., & Haussler, D. H. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0020033 · Cited by 515 · see citing works
The Elongation, Termination, and Recycling Phases of Translation in EukaryotesPreprint
Dever, T. E., & Green, R. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a013706 · Cited by 507 · see citing works
Translational control by the 3′-UTR: the ends specify the means
Mazumder, B., Seshadri, V., & Fox, P. L. (2003) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(03)00002-1 · Cited by 506 · see citing works
Introns and the origin of nucleus–cytosol compartmentalization
Martin, W. F., & Koonin, E. V. (2006) · Nature · doi:10.1038/nature04531 · Cited by 497 · see citing works
Formation, regulation and evolution of Caenorhabditis elegans 3′UTRs
Jan, C. H., Friedman, R. C., Ruby, J. G., & Bartel, D. P. (2010) · Nature · doi:10.1038/nature09616 · Cited by 482 · see citing works
The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif
Schaeffer, C., Bardoni, B., Mandel, J., Ehresmann, B., Ehresmann, C., & Moine, H. (2001) · The EMBO Journal · doi:10.1093/emboj/20.17.4803 · Cited by 471 · see citing works
Insights into RNA structure and function from genome-wide studies
Mortimer, S., Kidwell, M. A., & Doudna, J. A. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3681 · Cited by 465 · see citing works
DMS-MaPseq for genome-wide or targeted RNA structure probing in vivo
Zubradt, M. M., Gupta, P., Persad, S., Lambowitz, A. M., Weissman, J. S., & Rouskin, S. (2016) · Nature Methods · doi:10.1038/nmeth.4057 · Cited by 460 · see citing works
RNA G-Quadruplexes in Biology: Principles and Molecular Mechanisms
Fay, M. M., Lyons, S. M., & Ivanov, P. V. (2017) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.05.017 · Cited by 448 · see citing works
Transcriptome-wide distribution and function of RNA hydroxymethylcytosine
Delatte, B., Wang, F., Ngoc, L. V., Collignon, É., Bonvin, E., Deplus, R., Calonne, E., Hassabi, B., Putmans, P., Awe, S., et al. (2016) · Science · doi:10.1126/science.aac5253 · Cited by 441 · see citing works
The mammalian ribo-interactome reveals ribosome functional diversity and heterogeneity
Simsek, D., Tiu, G. C., Flynn, R. A., Byeon, G. W., Leppek, K., Xu, A. F., Chang, H. Y., & Barna, M. (2017) · Cell · doi:10.1016/j.cell.2017.05.022 · Cited by 439 · see citing works
Slobodin, B., Han, R., Calderone, V., Vrielink, J. A. F. O., Loayza-Puch, F., Elkon, R., & Agami, R. (2017) · Cell · doi:10.1016/j.cell.2017.03.031 · Cited by 434 · see citing works
Zhou, C., Molinié, B., Daneshvar, K., Pondick, J. V., Wang, J., Wittenberghe, N. V., Xing, Y., Giallourakis, C. C., & Mullen, A. C. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.027 · Cited by 430 · see citing works
eIF3 targets cell-proliferation messenger RNAs for translational activation or repression
Lee, A. S. Y., Kranzusch, P. J., & Cate, J. H. D. (2015) · Nature · doi:10.1038/nature14267 · Cited by 429 · see citing works
Structural and functional features of eukaryotic mRNA untranslated regions
Pesole, G., Mignone, F., Gissi, C., Grillo, G., Licciulli, F., & Liuni, S. (2001) · Gene · doi:10.1016/s0378-1119(01)00674-6 · Cited by 426 · see citing works
Cellular IRES-mediated translation
Komar, A. A., & Hatzoglou, M. (2011) · Cell Cycle · doi:10.4161/cc.10.2.14472 · Cited by 418 · see citing works
Structure and Thermodynamics of N 6 -Methyladenosine in RNA: A Spring-Loaded Base Modification
Roost, C., Lynch, S. R., Batista, P. J., Qu, K., Chang, H. Y., & Kool, E. T. (2015) · Journal of the American Chemical Society · doi:10.1021/ja513080v · Cited by 416 · see citing works
Cap and cap‐binding proteins in the control of gene expression
Topisirović, I., Svitkin, Y. V., Sonenberg, N., & Shatkin, A. J. (2010) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.52 · Cited by 402 · see citing works
Rousseau, D. L., Kaspar, R. L., Rosenwald, I. B., Gehrke, L., & Sonenberg, N. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.3.1065 · Cited by 401 · see citing works
A statistical test for conserved RNA structure shows lack of evidence for structure in lncRNAs
Rivas, E., Clements, J., & Eddy, S. R. (2016) · Nature Methods · doi:10.1038/nmeth.4066 · Cited by 363 · see citing works
Distinctive features of the 5′-terminal sequences of the human mitochondrial mRNAs
Montoya, J., Ojala, D., & Attardi, G. M. (1981) · Nature · doi:10.1038/290465a0 · Cited by 360 · see citing works
Programmed translational frameshifting
Farabaugh, P. J. (1996) · Microbiological Reviews · doi:10.1128/mr.60.1.103-134.1996 · Cited by 360 · see citing works
eIF3d is an mRNA cap-binding protein that is required for specialized translation initiation
Lee, A. S. Y., Kranzusch, P. J., Doudna, J. A., & Cate, J. H. D. (2016) · Nature · doi:10.1038/nature18954 · Cited by 358 · see citing works
Stoneley, M., & Willis, A. E. (2004) · Oncogene · doi:10.1038/sj.onc.1207551 · Cited by 353 · see citing works
Control of mammalian translation by mRNA structure near caps
Babendure, J. R., Babendure, J. L., Ding, J.-H., & Tsien, R. Y. (2006) · RNA · doi:10.1261/rna.2309906 · Cited by 339 · see citing works
Bordeleau, M.-È., Robert, F., Gerard, B., Lindqvist, L., Chen, S. M. H., Wendel, H., Brem, B., Greger, H., Lowe, S. W., Porco, J. A. J., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34753 · Cited by 335 · see citing works
Systematic discovery of cap-independent translation sequences in human and viral genomes
Weingarten-Gabbay, S., Elias-Kirma, S., Nir, R., Gritsenko, A. A., Stern-Ginossar, N., Yakhini, Z., Weinberger, A., & Segal, E. (2016) · Science · doi:10.1126/science.aad4939 · Cited by 334 · see citing works
A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting
Namy, O., Moran, S. J., Stuart, D. I., Gilbert, R. J. C., & Brierley, I. (2006) · Nature · doi:10.1038/nature04735 · Cited by 330 · see citing works
mRNA helicases: the tacticians of translational control
Parsyan, A., Svitkin, Y., Shahbazian, D., Gkogkas, C., Lasko, P., Merrick, W. C., & Sonenberg, N. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3083 · Cited by 323 · see citing works
RNA regulons in Hox 5′ UTRs confer ribosome specificity to gene regulation
Xue, S., Tian, S., Fujii, K., Kladwang, W., Das, R., & Barna, M. (2014) · Nature · doi:10.1038/nature14010 · Cited by 319 · see citing works
Self-citationJack, K. D., Bellodi, C., Landry, D. M., Niederer, R. O., Meškauskas, A., Musalgaonkar, S., Kopmar, N. E., Krasnykh, O., Dean, A. M., Thompson, S. R., et al. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.09.017 · Cited by 318 · see citing works
Wang, T., Martin, S., Nguyen, T. H., Harper, C. B., Gormal, R. S., Martínez‐Mármol, R., Karunanithi, S., Coulson, E. J., Glass, N. R., Cooper-White, J. J., et al. (2016) · Nature Communications · doi:10.1038/ncomms13768 · Cited by 316 · see citing works
The metabolism of a poly(A) minus mRNA fraction in HeLa cells
Milcarek, C., Price, R. P., & Penman, S. (1974) · Cell · doi:10.1016/0092-8674(74)90030-0 · Cited by 315 · see citing works
Rocaglates convert DEAD-box protein eIF4A into a sequence-selective translational repressor
Iwasaki, S., Floor, S. N., & Ingolia, N. T. (2016) · Nature · doi:10.1038/nature17978 · Cited by 304 · see citing works
Hinnebusch, A. G. (2017) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2017.03.004 · Cited by 304 · see citing works
Antitumor Activity and Mechanism of Action of the Cyclopenta[b]benzofuran, Silvestrol
Cencic, R., Carrier, M., Galicia-Vázquez, G., Bordeleau, M.-E., Sukarieh, R., Bourdeau, A., Brem, B., Teodoro, J. G., Greger, H., Tremblay, M. L., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005223 · Cited by 302 · see citing works
Muckenthaler, M., Gray, N. K., & Hentze, M. W. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80282-8 · Cited by 297 · see citing works
Re‐programming of translation following cell stress allows IRES‐mediated translation to predominate
Spriggs, K. A., Stoneley, M., Bushell, M., & Willis, A. E. (2007) · Biology of the Cell · doi:10.1042/bc20070098 · Cited by 292 · see citing works
Internal Ribosome Entry Sites in Cellular mRNAs: Mystery of Their Existence
Komar, A. A., & Hatzoglou, M. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.r400041200 · Cited by 288 · see citing works
Gray, N. K., & Hentze, M. W. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06699.x · Cited by 276 · see citing works
Before It Gets Started: Regulating Translation at the 5′ UTR
Araujo, P. R., Yoon, K., Ko, D., Smith, A. D., Qiao, M., Suresh, U., Burns, S. C., & Penalva, L. O. F. (2012) · Comparative and Functional Genomics · doi:10.1155/2012/475731 · Cited by 267 · see citing works
N6-methyladenosine in mRNA disrupts tRNA selection and translation-elongation dynamics
Choi, J., Ieong, K.-W., DeMi̇rci̇, H., Chen, J., Petrov, A. N., Prabhakar, A., O’Leary, S. E., Dominissini, D., Rechavi, G., Soltis, S. M., et al. (2016) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3148 · Cited by 260 · see citing works
Mitchell, S. A., Spriggs, K. A., Coldwell, M. J., Jackson, R. J., & Willis, A. E. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00093-5 · Cited by 259 · see citing works
5′-UTR G-quadruplex structures acting as translational repressors
Beaudoin, J.-D., & Perreault, J.-P. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq557 · Cited by 255 · see citing works
Translation initiation on mammalian mRNAs with structured 5′-UTRs requires DExH-box protein DHX29
Pisareva, V., Pisarev, A., Komar, A., Hellen, C., & Pestova, T. (2008) · Cell · doi:10.1016/j.cell.2008.10.037 · Cited by 241 · see citing works
Fragile X Mental Retardation Protein Regulates Translation by Binding Directly to the Ribosome
Chen, E., Sharma, M. R., Shi, X., Agrawal, R. K., & Joseph, S. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.03.023 · Cited by 240 · see citing works
Inhibition of translation in living eukaryotic cells by an RNA G-quadruplex motif
Arora, A., Dutkiewicz, M., Scaria, V., Hariharan, M., Maiti, S., & Kurreck, J. (2008) · RNA · doi:10.1261/rna.1001708 · Cited by 230 · see citing works
Genome-Wide Analysis of RNA Secondary Structure
Bevilacqua, P. C., Ritchey, L. E., Su, Z. Z., & Assmann, S. M. (2016) · Annual Review of Genetics · doi:10.1146/annurev-genet-120215-035034 · Cited by 222 · see citing works
RNA G-quadruplexes: emerging mechanisms in disease
Cammas, A., & Millevoi, S. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1280 · Cited by 219 · see citing works
Mechanisms and implications of programmed translational frameshifting
Dinman, J. D. (2012) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1126 · Cited by 210 · see citing works
IRESite—a tool for the examination of viral and cellular internal ribosome entry sites
Mokrejš, M., Mašek, T., Vopálenský, V., Hlubuček, P., Delbos, P., & Pospíšek, M. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp981 · Cited by 207 · see citing works
An RNA G-Quadruplex Is Essential for Cap-Independent Translation Initiation in Human VEGF IRES
Morris, M. J., Negishi, Y., Pazsint, C., et al. (2010) · Journal of the American Chemical Society · doi:10.1021/ja106287x · Cited by 207 · see citing works
Ben-Asouli, Y., Banai, Y., Pel-Or, Y., Shir, A., & Kaempfer, R. (2002) · Cell · doi:10.1016/s0092-8674(02)00616-5 · Cited by 206 · see citing works
The roles of RNA processing in translating genotype to phenotype
Manning, K. S., & Cooper, T. A. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.139 · Cited by 206 · see citing works
Principles of Translational ControlPreprint
Hershey, J. W. B., Sonenberg, N., & Mathews, M. B. (2018) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a032607 · Cited by 205 · see citing works
Chemical and structural effects of base modifications in messenger RNA
Harcourt, E. M., Kietrys, A. M., & Kool, E. T. (2017) · Nature · doi:10.1038/nature21351 · Cited by 201 · see citing works
Rubio, C. A., Weisburd, B., Holderfield, M., Arias, C., Fang, E., DeRisi, J. L., & Fanidi, A. (2014) · Genome Biology · doi:10.1186/s13059-014-0476-1 · Cited by 200 · see citing works
Gandin, V., Masvidal, L., Hulea, L., Gravel, S., Cargnello, M., McLaughlan, S., Cai, Y., Balanathan, P., Morita, M., Rajakumar, A., et al. (2016) · Genome Research · doi:10.1101/gr.197566.115 · Cited by 200 · see citing works
RNA-Puzzles Round III: 3D RNA structure prediction of five riboswitches and one ribozyme
Miao, Z.-C., Adamiak, R., Antczak, M., Batey, R., Becka, A. J., Biesiada, M., Boniecki, M. J., Bujnicki, J., Chen, S.-J., Cheng, C., et al. (2017) · RNA: A publication of the RNA Society · doi:10.1261/rna.060368.116 · Cited by 200 · see citing works
Self-citationA perspective on mammalian upstream open reading frame function
Somers, J., Pöyry, T. A. A., & Willis, A. E. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.04.020 · Cited by 199 · see citing works
The Zipper Model of Translational Control
Yaman, İ., Fernandez, J., Liu, H., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00345-3 · Cited by 199 · see citing works
The G-quartet containing FMRP binding site in FMR1 mRNA is a potent exonic splicing enhancer
Didiot, M.-C., Tian, Z., Schaeffer, C., Subramanian, M., Mandel, J., & Moine, H. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn472 · Cited by 196 · see citing works
RPS25 is essential for translation initiation by the Dicistroviridae and hepatitis C viral IRESsPreprint
Landry, D. M., Hertz, M. I., & Thompson, S. R. (2009) · Genes & Development · doi:10.1101/gad.1832209 · Cited by 195 · see citing works
Systematic discovery of structural elements governing stability of mammalian messenger RNAs
Goodarzi, H., Najafabadi, H. S., Oikonomou, P., Greco, T. M., Fish, L., Salavati, R., Cristea, I. M., & Tavazoie, S. (2012) · Nature · doi:10.1038/nature11013 · Cited by 187 · see citing works
Bonnal, S., Schaeffer, C., Créancier, L., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m305580200 · Cited by 182 · see citing works
Quantitative analysis of mammalian translation initiation sites by FACS‐seq
Noderer, W. L., Flockhart, R. J., Bhaduri, A., Diaz de Arce, A. J., Zhang, J., Khavari, P. A., & Wang, C. L. (2014) · Molecular Systems Biology · doi:10.15252/msb.20145136 · Cited by 178 · see citing works
Detection of RNA–Protein Interactions in Living Cells with SHAPE
Smola, M. J., Calabrese, J. M., & Weeks, K. M. (2015) · Biochemistry · doi:10.1021/acs.biochem.5b00977 · Cited by 175 · see citing works
Modelska, A., Turro, E., Russell, R. B., Beaton, J., Sbarrato, T., Spriggs, K. A., Miller, J. L., Gräf, S., Provenzano, E., Blows, F. M., et al. (2015) · Cell Death and Disease · doi:10.1038/cddis.2014.542 · Cited by 174 · see citing works
Sen, N. D., Zhou, F., Ingolia, N. T., et al. (2015) · Genome Research · doi:10.1101/gr.191601.115 · Cited by 170 · see citing works
Single-molecule correlated chemical probing of RNA
Homan, P., Favorov, O. V., Lavender, C. A., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1407306111 · Cited by 169 · see citing works
Operon mRNAs are organized into ORF-centric structures that predict translation efficiency
Burkhardt, D. H., Rouskin, S., Zhang, Y., Li, G., Weissman, J. S., & Gross, C. A. (2017) · eLife · doi:10.7554/elife.22037 · Cited by 163 · see citing works
FMRP interferes with the Rac1 pathway and controls actin cytoskeleton dynamics in murine fibroblasts
Castets, M., Schaeffer, C., Bechara, E., Schenck, A., Khandjian, E. W., Luche, S., Moine, H., Rabilloud, T., Mandel, J.-L., & Bardoni, B. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi077 · Cited by 162 · see citing works
Qin, X., & Sarnow, P. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m312854200 · Cited by 160 · see citing works
Variable chromatin structure revealed by in situ spatially correlated DNA cleavage mapping
Risca, V. I., Denny, S. K., Straight, A. F., & Greenleaf, W. J. (2016) · Nature · doi:10.1038/nature20781 · Cited by 159 · see citing works
The Current Status of Vertebrate Cellular mRNA IRESsPreprint
Jackson, R. J. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a011569 · Cited by 157 · see citing works
Regulation of rat ornithine decarboxylase mRNA translation by its 5'-untranslated region.
Manzella, J. M., & Blackshear, P. J. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)38471-6 · Cited by 154 · see citing works
Créancier, L., Morello, D., Mercier, P., & Prats, A. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.150.1.275 · Cited by 153 · see citing works
RNA G-quadruplexes and their potential regulatory roles in translation
Song, J., Perreault, J., Topisirović, I., & Richard, S. (2016) · Translation · doi:10.1080/21690731.2016.1244031 · Cited by 153 · see citing works
Morfoisse, F., Kuchnio, A., Frainay, C., Gomez‐Brouchet, A., Delisle, M., Marzi, S., Helfer, A., Hantelys, F., Pujol, F., Guillermet‐Guibert, J., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2013.12.011 · Cited by 145 · see citing works
The RNA structurome: transcriptome-wide structure probing with next-generation sequencing
Kwok, C. K., Tang, Y., Assmann, S. M., & Bevilacqua, P. C. (2015) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2015.02.005 · Cited by 144 · see citing works
RNA binding protein/RNA element interactions and the control of translation
Pichon, X., A. Wilson, L., Stoneley, M., Bastide, A., A King, H., Somers, J., & E Willis, A. (2012) · Current Protein & Peptide Science · doi:10.2174/138920312801619475 · Cited by 144 · see citing works
Lacerda, R., Menezes, J., & Romão, L. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2428-2 · Cited by 144 · see citing works
Mitchell, S. A., Spriggs, K. A., Bushell, M., Evans, J. R., Stoneley, M., Quesne, J. L., Spriggs, R. V., & Willis, A. (2005) · Genes & Development · doi:10.1101/gad.339105 · Cited by 142 · see citing works
Chappell, S. A., LeQuesne, J., Paulin, F., et al. (2000) · Oncogene · doi:10.1038/sj.onc.1203791 · Cited by 140 · see citing works
Schott, J., Reitter, S., Philipp, J., Haneke, K., Schäfer, H., & Stoecklin, G. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004368 · Cited by 136 · see citing works
Regulation of innate immunity through RNA structure and the protein kinase PKR
Nallagatla, S. R., Toroney, R., & Bevilacqua, P. C. (2010) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2010.11.003 · Cited by 133 · see citing works
Benhalevy, D., Gupta, S. K., Danan, C. H., Ghosal, S., Sun, H., Kazemier, H. G., Paeschke, K., Hafner, M., & Juranek, S. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.080 · Cited by 133 · see citing works
The role of IRES trans-acting factors in regulating translation initiation
King, H. A., Cobbold, L. C., & Willis, A. E. (2010) · Biochemical Society Transactions · doi:10.1042/bst0381581 · Cited by 132 · see citing works
RNA Sequence Context Effects Measured In Vitro Predict In Vivo Protein Binding and Regulation
Taliaferro, J. M., Lambert, N. J., Sudmant, P. H., Dominguez, D., Merkin, J. J., Alexis, M. S., Bazile, C. A., & Burge, C. B. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.08.035 · Cited by 130 · see citing works
Predictable suppression of gene expression by 5′-UTR-based RNA quadruplexes
Halder, K., Wieland, M., & Hartig, J. S. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp696 · Cited by 128 · see citing works
Evidence for a Functionally Relevant Rocaglamide Binding Site on the eIF4A–RNA Complex
Sadlish, H., Galicia-Vázquez, G., PARIS, C. G., Aust, T., Bhullar, B., Chang, L., Helliwell, S. B., Hoepfner, D., Knapp, B., Riedl, R., et al. (2013) · ACS Chemical Biology · doi:10.1021/cb400158t · Cited by 127 · see citing works
Computational Analysis of Conserved RNA Secondary Structure in Transcriptomes and Genomes
Eddy, S. R. (2014) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-051013-022950 · Cited by 127 · see citing works
Probing Xist RNA Structure in Cells Using Targeted Structure-Seq
Fang, R., Moss, W. N., Rutenberg-Schoenberg, M., et al. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005668 · Cited by 126 · see citing works
Dmitriev, S. E., Andreev, D. E., Terenin, I. M., Olovnikov, I. A., Prassolov, V., Merrick, W. C., & Shatsky, I. N. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02138-06 · Cited by 125 · see citing works
Kumari, S., Bugaut, A., & Balasubramanian, S. (2008) · Biochemistry · doi:10.1021/bi8010797 · Cited by 122 · see citing works
A two-dimensional mutate-and-map strategy for non-coding RNA structure
Kladwang, W., VanLang, C. C., Cordero, P., & Das, R. (2011) · Nature Chemistry · doi:10.1038/nchem.1176 · Cited by 121 · see citing works
Self-citation1 Origins and Principles of Translational ControlPreprint
Mathews, M. B., Sonenberg, N., & Hershey, J. W. B. (2007) · Cold Spring Harbor Monograph Archive · doi:10.1101/087969767.48.1 · Cited by 119 · see citing works
Tuning gene expression with synthetic upstream open reading frames
Ferreira, J. P., Overton, K. W., & Wang, C. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305590110 · Cited by 116 · see citing works
Osman, F., Jarrous, N., Ben-Asouli, Y., & Kaempfer, R. O. R. (1999) · Genes & Development · doi:10.1101/gad.13.24.3280 · Cited by 115 · see citing works
Duplex Unwinding and ATPase Activities of the DEAD-Box Helicase eIF4A Are Coupled by eIF4G and eIF4B
Özeş, A., Feoktistova, K., Avanzino, B. C., & Fraser, C. S. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.08.004 · Cited by 114 · see citing works
Parker, B. J., Moltke, I., Roth, A., Stefan Washietl, A., Wen, J., Kellis, M., Breaker, R. R., & Pedersen, J. S. (2011) · Genome Research · doi:10.1101/gr.112516.110 · Cited by 114 · see citing works
Molecular determinants and guided evolution of species-specific RNA editing
Reenan, R. A. (2005) · Nature · doi:10.1038/nature03364 · Cited by 112 · see citing works
Fernandez, J., Yaman, I., Merrick, W., Koromilas, A., Wek, R., Sood, R., Hensold, J., & Hatzoglou, M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m109199200 · Cited by 112 · see citing works
Cobbold, L. C., Wilson, L. A., Sawicka, K., King, H. A., Kondrashov, A. V., Spriggs, K. A., Bushell, M., & Willis, A. E. (2010) · Oncogene · doi:10.1038/onc.2010.31 · Cited by 106 · see citing works
Sen, N. D., Zhou, F., Harris, M. S., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1612398113 · Cited by 104 · see citing works
For IRES trans-acting factors, it is all about location
Lewis, S. M., & Holčı́k, M. (2007) · Oncogene · doi:10.1038/sj.onc.1210777 · Cited by 103 · see citing works
Progress and challenges for chemical probing of RNA structure inside living cells
Kubota, M., Tran, C., & Spitale, R. C. (2015) · Nature Chemical Biology · doi:10.1038/nchembio.1958 · Cited by 103 · see citing works
The Ribosome Challenge to the RNA World
Bowman, J. C., Hud, N. V., & Williams, L. D. (2015) · Journal of Molecular Evolution · doi:10.1007/s00239-015-9669-9 · Cited by 99 · see citing works
Thoma, C., Bergamini, G., Galy, B., Hundsdoerfer, P., & Hentze, M. W. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.08.021 · Cited by 95 · see citing works
Fernandez, J., Yaman, İ., Huang, C. Y., et al. (2005) · Molecular Cell · doi:10.1016/j.molcel.2004.12.024 · Cited by 94 · see citing works
Blau, L., Knirsh, R., Ben‐Dror, I., Oren, S., Kuphal, S., Hau, P., Proescholdt, M. A., Bosserhoff, A., & Vardimon, L. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1203659109 · Cited by 94 · see citing works
Derivation of a structural model for the c-myc IRES11Edited by J. Karn
Quesne, J. P. C. L., Stoneley, M., Fraser, G. A., & Willis, A. E. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4745 · Cited by 94 · see citing works
Pickering, B. M., Mitchell, S. A., Spriggs, K. A., Stoneley, M., & Willis, A. E. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.12.5595-5605.2004 · Cited by 94 · see citing works
Créancier, L., Mercier, P., Prats, A., & Morello, D. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.5.1833-1840.2001 · Cited by 93 · see citing works
A search for structurally similar cellular internal ribosome entry sites
Baird, S. D., Lewis, S. M., Turcotte, M., & Holčı́k, M. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm483 · Cited by 90 · see citing works
Conte, C., Riant, É., Toutain, C. E., Pujol, F., Arnal, J., Lenfant, F., & Prats, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003078 · Cited by 89 · see citing works
An upstream open reading frame within an IRES controls expression of a specific VEGF-A isoform
Bastide, A., Karaa, Z. S., Bornes, S., Hiéblot, C., Lacazette, É., Prats, H., & Touriol, C. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn093 · Cited by 85 · see citing works
Dynamic refolding of IFN-γ mRNA enables it to function as PKR activator and translation template
Cohen-Chalamish, S., Hasson, A., Weinberg, D., Namer, L. S., Banai, Y., Osman, F., & Kaempfer, R. (2009) · Nature Chemical Biology · doi:10.1038/nchembio.234 · Cited by 82 · see citing works
Pickering, B. M. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg146 · Cited by 81 · see citing works
Majumder, M., Yaman, İ., Gaccioli, F., Zeenko, V. V., Wang, C., Caprara, M. G., Venema, R. C., Komar, A. A., Snider, M. D., & Hatzoglou, M. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01774-08 · Cited by 81 · see citing works
The Evolution of Transcription-Initiation Sites
Lynch, M. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi100 · Cited by 81 · see citing works
Targeting the eIF4A RNA helicase as an anti-neoplastic approach
Chu, J., & Pelletier, J. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.09.006 · Cited by 80 · see citing works
Bouveret, R., Waardenberg, A. J., Schönrock, N., Ramialison, M., Doan, T. B., de Jong, D., Bondue, A., Kaur, G., Mohamed, S., Fonoudi, H., et al. (2015) · eLife · doi:10.7554/elife.06942 · Cited by 79 · see citing works
Origins and evolution of the mechanisms regulating translation initiation in eukaryotes
Hernández, G., Altmann, M., & Lasko, P. F. (2009) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2009.10.009 · Cited by 77 · see citing works
Splicing mediates the activity of four putative cellular internal ribosome entry sites
Baranick, B. T., Lemp, N. A., Nagashima, J., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710650105 · Cited by 76 · see citing works
Martineau, Y., Bec, C. L., Monbrun, L., Allo, V., Chiu, I., Danos, O., Moine, H., Prats, H., & Prats, A. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.17.7622-7635.2004 · Cited by 76 · see citing works
Cap-dependent, scanning-free translation initiation mechanisms
Haimov, O., Sinvani, H., & Dikstein, R. (2015) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2015.09.006 · Cited by 75 · see citing works
Stabilization of the G-quadruplex at the VEGF IRES represses cap-independent translation
Cammas, A., Dubrac, A., Morel, B., Lamaa, A., Touriol, C., Teulade‐Fichou, M., Prats, H., & Millevoi, S. (2015) · RNA Biology · doi:10.1080/15476286.2015.1017236 · Cited by 74 · see citing works
The role of G-quadruplex in RNA metabolism: involvement of FMRP and FMR2P
Melko, M., & Bardoni, B. (2010) · Biochimie · doi:10.1016/j.biochi.2010.05.018 · Cited by 74 · see citing works
Belew, A. T., Advani, V. M., & Dinman, J. D. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1220 · Cited by 74 · see citing works
Consistent global structures of complex RNA states through multidimensional chemical mapping
Cheng, C. Y., Chou, F., Kladwang, W., Tian, S., Cordero, P., & Das, R. (2015) · eLife · doi:10.7554/elife.07600 · Cited by 72 · see citing works
Self-citationRNA structure inference through chemical mapping after accidental or intentional mutations
Cheng, C. Y., Kladwang, W., Yesselman, J. D., & Das, R. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1619897114 · Cited by 68 · see citing works
Self-citationSahl, S. J., Lau, L., Vonk, W. I. M., Weiss, L. E., Frydman, J., & Moerner, W. E. (2015) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583515000219 · Cited by 66 · see citing works
Ribosomal 18S rRNA base pairs with mRNA during eukaryotic translation initiation
Martin, F., Ménétret, J., Simonetti, A., Myasnikov, A. G., Vicens, Q., Prongidi‐Fix, L., Natchiar, S. K., Klaholz, B. P., & Eriani, G. (2016) · Nature Communications · doi:10.1038/ncomms12622 · Cited by 62 · see citing works
Identification of consensus binding sites clarifies FMRP binding determinants
Anderson, B. R., Chopra, P., Suhl, J. A., Warren, S. T., & Bassell, G. J. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw593 · Cited by 59 · see citing works
RNA pseudoknots and the regulation of protein synthesis
Brierley, I., Gilbert, R. J. C., & Pennell, S. (2008) · Biochemical Society Transactions · doi:10.1042/bst0360684 · Cited by 58 · see citing works
Overexpression of FGF9 in colon cancer cells is mediated by hypoxia-induced translational activation
Chen, T.-M., Shih, Y.-H. J., Tseng, J. T., Lai, M., Wu, C.-H., Li, Y.-H., Tsai, S.-J., & Sun, H. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1286 · Cited by 58 · see citing works
High-throughput mutate-map-rescue evaluates SHAPE-directed RNA structure and uncovers excited states
Tian, S., Cordero, P., Kladwang, W., et al. (2014) · RNA · doi:10.1261/rna.044321.114 · Cited by 55 · see citing works
The role of IRES trans-acting factors in carcinogenesis
Faye, M. D., & Holčı́k, M. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.09.012 · Cited by 55 · see citing works
Advani, V. M., & Dinman, J. D. (2015) · BioEssays · doi:10.1002/bies.201500131 · Cited by 53 · see citing works
Irregular G-quadruplexes Found in the Untranslated Regions of Human mRNAs Influence Translation
Bolduc, F., Garant, J., Allard, F., & Perreault, J. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.744839 · Cited by 51 · see citing works
Gene regulation by structured mRNA elements
Wachter, A. (2014) · Trends in Genetics · doi:10.1016/j.tig.2014.03.001 · Cited by 49 · see citing works
A novel translational control mechanism involving RNA structures within coding sequencesPreprint
Jungfleisch, J., Nedialkova, D. D., Dotú, I., Sloan, K. E., Martínez‐Bosch, N., Brüning, L., Raineri, E., Navarro, P., Bohnsack, M. T., Leidel, S. A., et al. (2016) · Genome Research · doi:10.1101/gr.209015.116 · Cited by 49 · see citing works
RNA structure through multidimensional chemical mapping
Tian, S., & Das, R. (2016) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583516000020 · Cited by 47 · see citing works
Self-citationEvolution of the Protein Synthesis Machinery and Its Regulation
Cormier, P., Chassé, H., Cosson, B., et al. (2016) · Springer eBooks · doi:10.1007/978-3-319-39468-8 · Cited by 44 · see citing works
An Independently Folding RNA G-Quadruplex Domain Directly Recruits the 40S Ribosomal Subunit
Bhattacharyya, D., Diamond, P. D., & Basu, S. (2015) · Biochemistry · doi:10.1021/acs.biochem.5b00091 · Cited by 43 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
mRNA vaccines for infectious diseases: principles, delivery and clinical translation
Chaudhary, N., Weissman, D., & Whitehead, K. A. (2021) · Nature Reviews Drug Discovery · doi:10.1038/s41573-021-00283-5 · Cited by 1,555 · see citing works
Advances in COVID-19 mRNA vaccine development
Fang, E., Liu, X., Li, M., Zhang, Z., Song, L., Zhu, B., Wu, X., Liu, J., Zhao, D., & Li, Y. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00950-y · Cited by 601 · see citing works
The discovery of ribosome heterogeneity and its implications for gene regulation and organismal life
Genuth, N. R., & Barna, M. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.07.018 · Cited by 511 · see citing works
Self-citationThe promise of mRNA vaccines: a biotech and industrial perspective
Jackson, N. A. C., Kester, K. E., Casimiro, D., Gurunathan, S., & DeRosa, F. (2020) · npj Vaccines · doi:10.1038/s41541-020-0159-8 · Cited by 498 · see citing works
Human 5′ UTR design and variant effect prediction from a massively parallel translation assay
Sample, P. J., Wang, B., Reid, D. W., Presnyak, V., McFadyen, I. J., Morris, D. R., & Seelig, G. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0164-5 · Cited by 442 · see citing works
Combinatorial optimization of mRNA structure, stability, and translation for RNA-based therapeutics
Leppek, K., Byeon, G. W., Kladwang, W., Wayment-Steele, H. K., Kerr, C. H., Xu, A. F., Kim, D. S., Topkar, V. V., Choe, C., Rothschild, D., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28776-w · Cited by 399 · see citing works
Self-citationCombinatorial optimization of mRNA structure, stability, and translation for RNA-based therapeutics
Leppek, K., Byeon, G. W., Kladwang, W., Wayment-Steele, H. K., Kerr, C. H., Xu, A. F., Kim, D. S., Topkar, V. V., Choe, C., Rothschild, D., et al. (2021) · doi:10.1101/2021.03.29.437587 · Cited by 399 · see citing works
Self-citationNovel approaches for vaccine development
Gebre, M. S., Brito, L. A., Tostanoski, L. H., Edwards, D. K., Carfi, A., & Barouch, D. H. (2021) · Cell · doi:10.1016/j.cell.2021.02.030 · Cited by 347 · see citing works
Onabajo, O. O., Banday, A. R., Stanifer, M. L., Yan, W., Obajemu, A., Santer, D. M., Florez-Vargas, O., Piontkivska, H., Vargas, J. M., Ring, T. J., et al. (2020) · Nature Genetics · doi:10.1038/s41588-020-00731-9 · Cited by 261 · see citing works
Kim, S. C., Sekhon, S. S., Shin, W.-R., Ahn, G., Cho, B.-K., Ahn, J.-Y., & Kim, Y.-H. (2022) · Molecular & Cellular Toxicology · doi:10.1007/s13273-021-00171-4 · Cited by 255 · see citing works
A spatially resolved brain region- and cell type-specific isoform atlas of the postnatal mouse brain
Joglekar, A., Prjibelski, A., Mahfouz, A., Collier, P., Lin, S., Schlusche, A. K., Marrocco, J., Williams, S. R., Haase, B., Hayes, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20343-5 · Cited by 229 · see citing works
Cyclic GMP-AMP synthase promotes the inflammatory and autophagy responses in Huntington disease
Sharma, M., Rajendrarao, S., Shahani, N., Ramírez-Jarquín, U. N., & Subramaniam, S. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2002144117 · Cited by 155 · see citing works
Biomedical applications of mRNA nanomedicine
Xiong, Q., Lee, G. Y., Ding, J., Li, W., & Shi, J. (2018) · Nano Research · doi:10.1007/s12274-018-2146-1 · Cited by 125 · see citing works
Improved translation efficiency of therapeutic mRNA
Zarghampoor, F., Azarpira, N., Khatami, S. R., Behzad-Behbahani, A., & Foroughmand, A. M. (2019) · Gene · doi:10.1016/j.gene.2019.05.008 · Cited by 72 · see citing works
Crosstalk between G-quadruplex and ROS
Wu, S., Jiang, L., Lei, L., Fu, C., Huang, J., Hu, Y., Dong, Y., Chen, J., & Zeng, Q. (2023) · Cell Death & Disease · doi:10.1038/s41419-023-05562-0 · Cited by 69 · see citing works
“For instance, the G4 structure in the 5′UTR plays a regulatory role in translation [154].”
BackgroundPredicting the translation efficiency of messenger RNA in mammalian cells
Zheng, D., Persyn, L., Wang, J., Liu, Y., Ulloa-Montoya, F., Cenik, C., & Agarwal, V. (2026) · Nature Biotechnology · doi:10.1038/s41587-025-02712-x · Cited by 52 · see citing works
Targeting Translation of mRNA as a Therapeutic Strategy in Cancer
Pal, I., Safari, M., Jovanovic, M., Bates, S. E., & Deng, C. (2019) · Current Hematologic Malignancy Reports · doi:10.1007/s11899-019-00530-y · Cited by 46 · see citing works
Effects of Combinations of Untranslated-Region Sequences on Translation of mRNA
Kirshina, A., Vasileva, O., Kunyk, D., Seregina, K., Muslimov, A., Ivanov, R., & Reshetnikov, V. (2023) · Biomolecules · doi:10.3390/biom13111677 · Cited by 26 · see citing works
Advancing mRNA technologies for therapies and vaccines: An African context
Kairuz, D., Samudh, N., Ely, A., Arbuthnot, P., & Bloom, K. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1018961 · Cited by 25 · see citing works
“Mammalian 5’ UTRs vary greatly in length and secondary structure with longer, and more structurally stable UTRs correlating with reduced capdependent ribosome scanning and translation efficiency ( (36); reviewed in (21)).”
BackgroundIdentification of novel 5’ UTR variants for enhanced mRNA translation and vaccine immunogenicity
Mazunina, E. P., Dzharullaeva, A. S., Kleymenov, D. A., Bykonia, E. N., Kozlova, S. R., Usachev, E. V., Panova, E. A., Konopleva, M. V., Telegina, D. V., Kukushkina-Zvezdova, A. A., et al. (2026) · Scientific Reports · doi:10.1038/s41598-026-59586-5
- Authors
- Leppek, K., Das, R., & Barna, M.
- Affiliations
- Stanford University (US)
- Corresponding author
- Das, Rhiju
- Barna, Maria
- Venue
- Nature Reviews Molecular Cell Biology
- Published
- 2017-11-22
- Volume
- 19
- Issue
- 3
- Pages
- 158-174
- ISSN
- 1471-0072 (ISSN-L)
- 1471-0080
- PMC
- PMC5820134
- OpenAlex
- W2770378609
- Cited by
- 949
- References
- 209
- Citations by year
- 2026: 109 · 2025: 145 · 2024: 139 · 2023: 112 · 2022: 129 · 2021: 111 · 2020: 102 · 2019: 62 · 2018: 40
- FWCI
- 5.22
- Type
- journal article
- Language
- en
- Update notices
- correction (2018-08-15)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Reviews Molecular Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (R01GM102519, R35GM122579)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21HD086730, R01HD086634)
- Topics
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
- Keywords
- 5' untranslated region, mRNA structure, translation initiation, cap-dependent translation, cap-independent translation, internal ribosome entry site, RNA structure probing, post-transcriptional regulation, RNA helicase, mRNA modification
- MeSH terms
- Internal Ribosome Entry Sites, Animals, Humans, Models, Biological, Models, Molecular, Peptide Chain Initiation, Translational, Ribosomes, RNA, Messenger, Protein Biosynthesis, 5' Untranslated Regions, RNA Helicases, Eukaryotic Initiation Factor-4F, Eukaryotic Initiation Factor-3, G-Quadruplexes, RNA Folding
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