Characterizing expression and processing of precursor and mature human tRNAs by hydro-tRNAseq and PAR-CLIP
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The participation of tRNAs in fundamental aspects of biology and disease necessitates an accurate, experimentally confirmed annotation of tRNA genes and curation of tRNA sequences. This has been challenging because RNA secondary structure, nucleotide modifications, and tRNA gene multiplicity complicate sequencing and mapping efforts. To address these issues, we developed hydro-tRNAseq, a method based on partial alkaline RNA hydrolysis that generates fragments amenable for sequencing. To identify transcribed tRNA genes, we further complemented this approach with photoactivatable crosslinking and immunoprecipitation (PAR-CLIP) of SSB/La, a conserved protein involved in pre-tRNA processing. Our results show that approximately half of all predicted tRNA genes are transcribed in human cells. We also report nucleotide modification sites and their order of introduction, and we identify tRNA leaders, trailers, and introns. By using complementary sequencing-based methodologies, we present a human tRNA atlas and determine expression levels of mature and processing intermediates of tRNAs in human cells.
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High-throughput tRNA-specific sequencing techniques have been developed.
“More recently, high-throughput tRNA-specific sequencing techniques have also been developed.”
From Role of host tRNAs and aminoacyl-tRNA synthetases in retroviral replication (2019) · cites this paper as [140]
A hydrolysis-based tRNA sequencing method allowed detection of tRNA precursors.
“A hydrolysis-based tRNA sequencing method further allowed detection of tRNA precursors (140).”
From Role of host tRNAs and aminoacyl-tRNA synthetases in retroviral replication (2019) · cites this paper as [140]
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Synonymous but not the same: the causes and consequences of codon bias
Plotkin, J. B., & Kudla, G. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2899 · Cited by 1,677 · see citing works
The mRNA-Bound Proteome and Its Global Occupancy Profile on Protein-Coding Transcripts
Baltz, A. G., Munschauer, M., Schwanhäußer, B., Vasile, A. I., Murakawa, Y., Schueler, M., Youngs, N., Penfold-Brown, D., Drew, K., Milek, M., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.05.021 · Cited by 1,175 · see citing works
A novel class of small RNAs: tRNA-derived RNA fragments (tRFs)
Lee, Y. S., Shibata, Y., Malhotra, A., & Dutta, A. (2009) · Genes & Development · doi:10.1101/gad.1837609 · Cited by 1,066 · see citing works
MODOMICS: a database of RNA modification pathways—2013 update
Machnicka, M. A., Milanowska, K., Oglou, O. O., Purta, E., Kurkowska, M., Olchowik, A., Januszewski, W., Kalinowski, S., Dunin-Horkawicz, S., Rother, K. M., et al. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1007 · Cited by 1,003 · see citing works
Angiogenin-Induced tRNA Fragments Inhibit Translation Initiation
Ivanov, P. V., Emara, M. M., Villén, J., Gygi, S. P., & Anderson, P. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.06.022 · Cited by 986 · see citing works
An evolutionarily conserved mechanism for controlling the efficiency of protein translation
Tuller, T., Carmi, A., Vestsigian, K., Navon, S., Dorfan, Y., Zaborske, J., Pan, T., Dahan, O., Furman, I., & Pilpel, Y. (2010) · Cell · doi:10.1016/j.cell.2010.03.031 · Cited by 874 · see citing works
tRNAdb 2009: compilation of tRNA sequences and tRNA genes
Jühling, F., Mörl, M., Hartmann, R. K., Sprinzl, M., Stadler, P. F., & Pütz, J. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn772 · Cited by 848 · see citing works
tRNA biology charges to the frontPreprint
Phizicky, E. M., & Hopper, A. K. (2010) · Genes & Development · doi:10.1101/gad.1956510 · Cited by 764 · see citing works
Efficient and quantitative high-throughput tRNA sequencing
Zheng, G., Qin, Y., Clark, W. C., Dai, Q., Yi, C., He, C., Lambowitz, A. M., & Pan, T. (2015) · Nature Methods · doi:10.1038/nmeth.3478 · Cited by 550 · see citing works
Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding
Pechmann, S., & Frydman, J. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2466 · Cited by 487 · see citing works
A Dual Program for Translation Regulation in Cellular Proliferation and Differentiation
Gingold, H., Tehler, D., Christoffersen, N. R., Nielsen, M. M., Asmar, F., Kooistra, S. M., Christophersen, N. S., Christensen, L. L., Borre, M., Sørensen, K. D., et al. (2014) · Cell · doi:10.1016/j.cell.2014.08.011 · Cited by 487 · see citing works
Cozen, A. E., Quartley, E., Holmes, A. D., Hrabeta-Robinson, E., Phizicky, E. M., & Lowe, T. M. (2015) · Nature Methods · doi:10.1038/nmeth.3508 · Cited by 479 · see citing works
Modulated Expression of Specific tRNAs Drives Gene Expression and Cancer Progression
Goodarzi, H., Nguyen, H. C. B., Zhang, S., Dill, B. D., Molina, H., & Tavazoie, S. F. (2016) · Cell · doi:10.1016/j.cell.2016.05.046 · Cited by 454 · see citing works
Weinberg, D. E., Shah, P., Eichhorn, S. W., Hussmann, J. A., Plotkin, J. B., & Bartel, D. P. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.043 · Cited by 392 · see citing works
Stefano, J. E. (1984) · Cell · doi:10.1016/0092-8674(84)90083-7 · Cited by 375 · see citing works
The genetic code : the molecular basis for genetic expression
Woese, C. R. (1967) · Harper & Row eBooks · Cited by 295 · see citing works
Oler, A. J., Alla, R., Roberts, D. N., Wong, A., Hollenhorst, P. C., Chandler, K. J., Cassiday, P. A., Nelson, C. A., Hagedorn, C. H., Graves, B. J., et al. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1801 · Cited by 282 · see citing works
The Genetic Code. The Molecular Basis for Genetic Expression
WOOLF, L. I. (1968) · Journal of Medical Genetics · doi:10.1136/jmg.5.2.159 · Cited by 282 · see citing works
Schaffer, A. E., Eggens, V. R., Çağlayan, A. O., Reuter, M. S., Scott, E., Coufal, N. G., Silhavy, J. L., Xue, Y., Kayserili, H., Yasuno, K., et al. (2014) · Cell · doi:10.1016/j.cell.2014.03.049 · Cited by 273 · see citing works
Moqtaderi, Z., Wang, J., Raha, D., White, R. J., Snyder, M. P., Weng, Z., & Struhl, K. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1794 · Cited by 230 · see citing works
Karaca, E., Weitzer, S., Pehli̇van, D., Shiraishi, H., Gogakos, T., Hanada, T., Jhangiani, S. N., Wiszniewski, W. K., Withers, M. A., Campbell, I. M., et al. (2014) · Cell · doi:10.1016/j.cell.2014.02.058 · Cited by 209 · see citing works
Self-citationClassification, diagnosis and potential mechanisms in Pontocerebellar Hypoplasia
Namavar, Y., Barth, P. G., Poll‐The, B. T., & Baas, F. (2011) · Orphanet Journal of Rare Diseases · doi:10.1186/1750-1172-6-50 · Cited by 178 · see citing works
Conserved and divergent features of the structure and function of La and La-related proteins (LARPs)
Bayfield, M. A., Yang, R., & Maraia, R. J. (2010) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2010.01.011 · Cited by 164 · see citing works
Teplova, M., Yuan, Y.-R., Phan, A. T., Malinina, L. V., Ilin, S., Теплов, А. А., & Patel, D. J. (2006) · Molecular Cell · doi:10.1016/j.molcel.2005.10.027 · Cited by 158 · see citing works
Mechanism of Eukaryotic RNA Polymerase III Transcription Termination
Nielsen, S., Yuzenkova, Y., & Zenkin, N. (2013) · Science · doi:10.1126/science.1237934 · Cited by 141 · see citing works
3′ processing of eukaryotic precursor tRNAs
Maraia, R. J., & Lamichhane, T. N. (2010) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.64 · Cited by 131 · see citing works
The Lupus Autoantigen La Prevents Mis-channeling of tRNA Fragments into the Human MicroRNA Pathway
Hasler, D., Lehmann, G. J., Murakawa, Y., Klironomos, F., Jakob, L., Grässer, F. A., Rajewsky, N., Landthaler, M., & Meister, G. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.05.026 · Cited by 128 · see citing works
YAMAT-seq: an efficient method for high-throughput sequencing of mature transfer RNAs
Shigematsu, M., Honda, S., Loher, P., Telonis, A. G., Rigoutsos, I., & Kirino, Y. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx005 · Cited by 125 · see citing works
Inosine modifications in human tRNAs are incorporated at the precursor tRNA level
Torres, A. G., Piñeyro, D., Rodríguez-Escribà, M., Camacho, N., Reina, Ó., Saint-Léger, A., Filonava, L., Batlle, E., & de Pouplana, L. R. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv277 · Cited by 115 · see citing works
Barcoded cDNA library preparation for small RNA profiling by next-generation sequencing
Hafner, M., Renwick, N. M., Farazi, T. A., Mihailović, A., Pena, J., & Tuschl, T. (2012) · Methods · doi:10.1016/j.ymeth.2012.07.030 · Cited by 114 · see citing works
Self-citationDana, A., & Tuller, T. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002755 · Cited by 111 · see citing works
Kutter, C., Brown, G. D., Gonçalves, Â., Wilson, M. D., Watt, S., Brāzma, A., White, R. J., & Odom, D. T. (2011) · Nature Genetics · doi:10.1038/ng.906 · Cited by 109 · see citing works
Gu, W., Jackman, J. E., Lohan, A. J., Gray, M. W., & Phizicky, E. M. (2003) · Genes & Development · doi:10.1101/gad.1148603 · Cited by 108 · see citing works
Exploring the Regulation of tRNA Distribution on the Genomic Scale
Dittmar, K. A., Mobley, E. M., Radek, A. J., & Pan, T. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.01.024 · Cited by 94 · see citing works
Arimbasseri, G. A., & Maraia, R. J. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.04.002 · Cited by 87 · see citing works
RNA Polymerase III Output Is Functionally Linked to tRNA Dimethyl-G26 Modification
Arimbasseri, G. A., Blewett, N. H., Iben, J., Lamichhane, T. N., Cherkasova, V. A., Hafner, M., & Maraia, R. J. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005671 · Cited by 85 · see citing works
Self-citationArimbasseri, G. A., Iben, J., Wei, F., Rijal, K., Tomizawa, K., Hafner, M., & Maraia, R. J. (2016) · RNA · doi:10.1261/rna.056259.116 · Cited by 80 · see citing works
Self-citationtRNA gene copy number variation in humans
Iben, J., & Maraia, R. J. (2013) · Gene · doi:10.1016/j.gene.2013.11.049 · Cited by 71 · see citing works
Precursor-product discrimination by La protein during tRNA metabolism
Bayfield, M. A., & Maraia, R. J. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1573 · Cited by 61 · see citing works
Garzia, A., Meyer, C., Morozov, P. S., Sajek, M. P., & Tuschl, T. (2016) · Methods · doi:10.1016/j.ymeth.2016.10.007 · Cited by 59 · see citing works
Self-citationThe La Protein-RNA Complex Surfaces
Maraia, R. J., & Bayfield, M. A. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.01.004 · Cited by 56 · see citing works
Dana, A., & Tuller, T. (2014) · G3 Genes Genomes Genetics · doi:10.1534/g3.114.015099 · Cited by 53 · see citing works
Iben, J., & Maraia, R. J. (2012) · RNA · doi:10.1261/rna.032151.111 · Cited by 51 · see citing works
Conservation of the relative tRNA composition in healthy and cancerous tissues
Mahlab-Aviv, S., Tuller, T., & Michal Linial, B. (2012) · RNA · doi:10.1261/rna.030775.111 · Cited by 47 · see citing works
Control of Saccharomyces cerevisiae pre-tRNA processing by environmental conditions
Foretek, D., Wu, J., Hopper, A. K., & Boguta, M. (2016) · RNA · doi:10.1261/rna.054973.115 · Cited by 33 · see citing works
Spitzer, J., Landthaler, M., & Tuschl, T. (2013) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-418687-3.00008-2 · Cited by 31 · see citing works
Self-citationDistinguishing Core and Holoenzyme Mechanisms of Transcription Termination by RNA Polymerase III
Arimbasseri, G. A., & Maraia, R. J. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01733-12 · Cited by 27 · see citing works
Comment on “Mechanism of eukaryotic RNA polymerase III transcription termination”
Arimbasseri, G. A., Kassavetis, G. A., & Maraia, R. J. (2014) · Science · doi:10.1126/science.1253783 · Cited by 24 · see citing works
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Translation affects mRNA stability in a codon-dependent manner in human cells
Wu, Q., Medina, S. G., Kushawah, G., DeVore, M. L., Castellano, L. A., Hand, J. M., Wright, M., & Bazzini, A. A. (2019) · eLife · doi:10.7554/elife.45396 · Cited by 283 · see citing works
Behrens, A., Rodschinka, G., & Nedialkova, D. D. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.01.028 · Cited by 248 · see citing works
Noncanonical Roles of tRNAs: tRNA Fragments and Beyond
Su, Z., Wilson, B., Kumar, P., & Dutta, A. (2020) · Annual Review of Genetics · doi:10.1146/annurev-genet-022620-101840 · Cited by 241 · see citing works
Quantitative analysis of tRNA abundance and modifications by nanopore RNA sequencing
Lucas, M. C., Pryszcz, L. P., Medina, R., Milenkovic, I., Camacho, N., Marchand, V., Motorin, Y., de Pouplana, L. R., & Novoa, E. M. (2023) · Nature Biotechnology · doi:10.1038/s41587-023-01743-6 · Cited by 229 · see citing works
Das, S., Abdel‐Mageed, A. B., Adamidi, C., Adelson, P. D., Akat, K. M., Alsop, E. B., Ansel, K. M., Arango, J. I., D, N. A. M., Kilinc, S., et al. (2019) · Cell · doi:10.1016/j.cell.2019.03.023 · Cited by 223 · see citing works
Self-citationDifferential expression of human tRNA genes drives the abundance of tRNA-derived fragments
Torres, A. G., Reina, Ó., Attolini, C. S., & de Pouplana, L. R. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1821120116 · Cited by 182 · see citing works
Quantitative tRNA-sequencing uncovers metazoan tissue-specific tRNA regulation
Pinkard, O. W., McFarland, S., Sweet, T. J., & Coller, J. M. (2020) · Nature Communications · doi:10.1038/s41467-020-17879-x · Cited by 178 · see citing works
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Orellana, E. A., Siegal, E. Z., & Gregory, R. I. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00501-9 · Cited by 175 · see citing works
Matching tRNA modifications in humans to their known and predicted enzymes
de Crécy‐Lagard, V., Boccaletto, P., Mangleburg, C. G., Sharma, P., Lowe, T. M., Leidel, S. A., & Bujnicki, J. M. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz011 · Cited by 170 · see citing works
Mo, D., Jiang, P., Yang, Y., Mao, X., Xuyan, T., Tang, X., Wei, D., Li, B., Wang, X., Tang, L. P., et al. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.05.007 · Cited by 166 · see citing works
Engineered transfer RNAs for suppression of premature termination codons
Lueck, J. D., Yoon, J. S., Perales‐Puchalt, A., Mackey, A. L., Infield, D. T., Behlke, M. A., Pope, M. R., Weiner, D. B., Skach, W. R., McCray, P. B., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08329-4 · Cited by 158 · see citing works
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Fragmentation of extracellular ribosomes and tRNAs shapes the extracellular RNAome
Tosar, J. P., Segovia, M., Castellano, M., Gámbaro, F., Akiyama, Y., Fagúndez, P., Olivera, Á., Costa, B., Possi, T., Hill, M., et al. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa674 · Cited by 106 · see citing works
Blaze, J., Navickas, A., Phillips, H. L., Heissel, S., Plaza-Jennings, A. L., Miglani, S., Asgharian, H., Foo, M., Katanski, C. D., Watkins, C. P., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24969-x · Cited by 95 · see citing works
Epitranscriptome: Review of Top 25 Most-Studied RNA Modifications
Arzumanian, V. A., Dolgalev, G. V., Kurbatov, I. Y., Kiseleva, O. I., & Poverennaya, E. V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232213851 · Cited by 94 · see citing works
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Schaffer, A. E., Pinkard, O. W., & Coller, J. M. (2019) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-083118-015334 · Cited by 92 · see citing works
Proximity-CLIP provides a snapshot of protein-occupied RNA elements in subcellular compartments
Benhalevy, D., Anastasakis, D. G., & Hafner, M. (2018) · Nature Methods · doi:10.1038/s41592-018-0220-y · Cited by 91 · see citing works
Self-citationTosar, J. P., Gámbaro, F., Darré, L., Pantano, S., Westhof, É., & Cayota, A. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky495 · Cited by 89 · see citing works
Quantitative mapping of the cellular small RNA landscape with AQRNA-seq
Hu, J. F., Yim, D., Ma, D., Huber, S. M., Davis, N., Bacusmo, J. M., Vermeulen, S. Y., Zhou, J., Begley, T. J., DeMott, M. S., et al. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00874-y · Cited by 83 · see citing works
Interchangeable parts: The evolutionarily dynamic tRNA population in plant mitochondria
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Thrun, A., Garzia, A., Kigoshi-Tansho, Y., Patil, P. R., Umbaugh, C. S., Dallinger, T., Liu, J., Kreger, S., Patrizi, A., Cox, G. A., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.03.004 · Cited by 77 · see citing works
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Evasion of antiviral bacterial immunity by phage tRNAs
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Wen, J.-T., Huang, Z., Li, Q., Chen, X., Qin, H., & Zhao, Y. (2021) · Cell Death Discovery · doi:10.1038/s41420-021-00789-2 · Cited by 75 · see citing works
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Pathways to disease from natural variations in human cytoplasmic tRNAs
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A rare codon-based translational program of cell proliferation
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tRNA therapeutics for genetic diseases
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Regulation of La/SSB-dependent viral gene expression by pre-tRNA 3′ trailer-derived tRNA fragments
Cho, H., Lee, W., Kim, G., Lee, S., Moon, J.-S., Kim, M., Kim, H. S., & Oh, J. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz732 · Cited by 70 · see citing works
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Gerber, A., Ito, K., Chu, C.-S., & Roeder, R. G. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.03.023 · Cited by 68 · see citing works
Role of host tRNAs and aminoacyl-tRNA synthetases in retroviral replication
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“A hydrolysis-based tRNA sequencing method further allowed detection of tRNA precursors (140).”
MethodFagan, S. G., Helm, M., & Prehn, J. H. M. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102118 · Cited by 67 · see citing works
RNA Polymerase III Subunit Mutations in Genetic Diseases
Lata, E., Choquet, K., Sagliocco, F. A., Brais, B., Bernard, G., & Teichmann, M. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.696438 · Cited by 65 · see citing works
Translational efficiency across healthy and tumor tissues is proliferation‐related
Hernandez‐Alias, X., Benisty, H., Schaefer, M. H., & Serrano, L. G. (2020) · Molecular Systems Biology · doi:10.15252/msb.20199275 · Cited by 64 · see citing works
Microbiome characterization by high-throughput transfer RNA sequencing and modification analysis
Schwartz, M. H., Wang, H., Pan, J. N., Clark, W. C., Cui, S., Eckwahl, M. J., Pan, D. W., Parisien, M., Owens, S. M., Cheng, B. L., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07675-z · Cited by 59 · see citing works
Choquet, K., Forget, D., Meloche, E., Dicaire, M., Bernard, G., Vanderver, A. L., Schiffmann, R., Fabian, M. R., Teichmann, M., Coulombe, B., et al. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006271 · Cited by 58 · see citing works
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Macken, W. L., Vandrovcová, J., Hanna, M. G., & Pitceathly, R. D. S. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-021-00455-2 · Cited by 56 · see citing works
Inferring targeting modes of Argonaute-loaded tRNA fragments
Guan, L.-Y., Karaiskos, S., & Grigoriev, A. (2019) · RNA Biology · doi:10.1080/15476286.2019.1676633 · Cited by 54 · see citing works
CoCo: RNA-seq read assignment correction for nested genes and multimapped reads
Deschamps-Francoeur, G., Boivin, V., Elela, S. A., & Scott, M. S. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz433 · Cited by 54 · see citing works
Gobet, C., Weger, B. D., Marquis, J., Martín, E., Neelagandan, N., Gachon, F., & Naef, F. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1918145117 · Cited by 54 · see citing works
Transfer RNAs as dynamic and critical regulators of cancer progression
Pinzaru, A. M., & Tavazoie, S. F. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00611-4 · Cited by 53 · see citing works
Hijacking tRNAs From Translation: Regulatory Functions of tRNAs in Mammalian Cell Physiology
Avcilar-Kücükgöze, I., & Kashina, A. S. (2020) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2020.610617 · Cited by 53 · see citing works
Predicting 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
Hayne, C. K., Schmidt, C. A., Haque, M. I., Matera, A. G., & Stanley, R. E. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa438 · Cited by 52 · see citing works
Asanović, I., Strandback, E., Kroupova, A., Pasajlic, D., Meinhart, A., Pai, T., Djoković, N., Anrather, D., Schuetz, T., Suskiewicz, M. J., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.04.007 · Cited by 51 · see citing works
Mattijssen, S., Arimbasseri, G. A., Iben, J., Gaidamakov, S., Lee, J., Hafner, M., & Maraia, R. J. (2017) · eLife · doi:10.7554/elife.28889 · Cited by 50 · see citing works
Self-citationYamagami, R., Sieg, J. P., Assmann, S. M., & Bevilacqua, P. C. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2201237119 · Cited by 49 · see citing works
Decoding protein–RNA interactions using CLIP-based methodologies
Xiang, J. S., Schafer, D. M., Rothamel, K. L., & Yeo, G. W.-M. (2024) · Nature Reviews Genetics · doi:10.1038/s41576-024-00749-3 · Cited by 48 · see citing works
Tie-Break: Host and Retrotransposons Play tRNA
Schorn, A. J., & Martienssen, R. A. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.05.006 · Cited by 48 · see citing works
van Ingen, E., Engbers, P. A. M., Woudenberg, T., van der Bent, M. L., Mei, H., Wojta, J., Quax, P. H. A., & Nossent, A. Y. (2022) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2022.09.011 · Cited by 47 · see citing works
Advances in methods for tRNA sequencing and quantification
Padhiar, N. H., Katneni, U., Komar, A. A., Motorin, Y., & Kimchi‐Sarfaty, C. (2023) · Trends in Genetics · doi:10.1016/j.tig.2023.11.001 · Cited by 46 · see citing works
Enjoy the Silence: Nearly Half of Human tRNA Genes Are Silent
Torres, A. G. (2019) · Bioinformatics and Biology Insights · doi:10.1177/1177932219868454 · Cited by 46 · see citing works
Translational adaptation of human viruses to the tissues they infect
Hernandez‐Alias, X., Benisty, H., Schaefer, M. H., & Serrano, L. G. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108872 · Cited by 45 · see citing works
Roles and dynamics of 3-methylcytidine in cellular RNAs
Bohnsack, K. E., Kleiber, N., Lemus-Diaz, N., & Bohnsack, M. T. (2022) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2022.03.004 · Cited by 44 · see citing works
Threonine fuels glioblastoma through YRDC-mediated codon-biased translational reprogramming
Wu, X., Yuan, H., Wu, Q., Gao, Y., Duan, T., Yang, K., Huang, T., Wang, S., Yuan, F., Lee, D., et al. (2024) · Nature Cancer · doi:10.1038/s43018-024-00748-7 · Cited by 44 · see citing works
Erber, L., Hoffmann, A., Fallmann, J., Betat, H., Stadler, P. F., & Mörl, M. (2019) · RNA Biology · doi:10.1080/15476286.2019.1664250 · Cited by 44 · see citing works
Huh, D., Passarelli, M. C., Gao, J., Dusmatova, S. N., Goin, C., Fish, L., Pinzaru, A. M., Molina, H., Ren, Z., McMillan, E. A., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2020106696 · Cited by 43 · see citing works
ELAC1 Repairs tRNAs Cleaved during Ribosome-Associated Quality Control
Yip, M. C. J., Savickas, S., Gygi, S. P., & Shao, S. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.082 · Cited by 42 · see citing works
Epigenetic regulation of human non-coding RNA gene transcription
Morselli, M., & Dieci, G. (2022) · Biochemical Society Transactions · doi:10.1042/bst20210860 · Cited by 43 · see citing works
Velcrin-induced selective cleavage of tRNALeu(TAA) by SLFN12 causes cancer cell death
Lee, S., Hoyt, S. H., Wu, X., Garvie, C. W., McGaunn, J. P., Shekhar, M., Tötzl, M., Rees, M. G., Cherniack, A. D., Meyerson, M. M., et al. (2022) · Nature Chemical Biology · doi:10.1038/s41589-022-01170-9 · Cited by 41 · see citing works
Reducing the structure bias of RNA-Seq reveals a large number of non-annotated non-coding RNA
Boivin, V., Reulet, G., Boisvert, O., Couture, S., Elela, S. A., & Scott, M. S. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa028 · Cited by 41 · see citing works
Cell-type-specific expression of tRNAs in the brain regulates cellular homeostasis
Kapur, M., Molumby, M. J., Guzman, C., Heinz, S., & Ackerman, S. L. (2024) · Neuron · doi:10.1016/j.neuron.2024.01.028 · Cited by 40 · see citing works
Predicting transfer RNA gene activity from sequence and genome contextPreprint
Thornlow, B. P., Armstrong, J. C., Holmes, A., Howard, J. M., Corbett-Detig, R. B., & Lowe, T. M. (2019) · Genome Research · doi:10.1101/gr.256164.119 · Cited by 40 · see citing works
ALL-tRNAseq enables robust tRNA profiling in tissue samplesPreprint
Scheepbouwer, C., Aparicio‐Puerta, E., Gómez‐Martín, C., Verschueren, H., van Eijndhoven, M. A. J., Wedekind, L. E., Giannoukakos, S., Hijmering, N. J., Gasparotto, L., van der Galiën, H. T., et al. (2023) · Genes & Development · doi:10.1101/gad.350233.122 · Cited by 40 · see citing works
Kuo, M. E., & Antonellis, A. (2019) · Trends in Genetics · doi:10.1016/j.tig.2019.11.007 · Cited by 39 · see citing works
Sekulovski, S., Devant, P., Panizza, S., Gogakos, T., Pitiriciu, A., Heitmeier, K., Ramsay, E. P., Barth, M., Schmidt, C., Tuschl, T., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25870-3 · Cited by 39 · see citing works
Self-citationAbsolute Quantification of Noncoding RNA by Microscale Thermophoresis
Jacob, D., Thüring, K. L., Galliot, A., Marchand, V., Galvanin, A., Ciftci, A., Scharmann, K., Stock, M., Roignant, J., Leidel, S. A., et al. (2019) · Angewandte Chemie International Edition · doi:10.1002/anie.201814377 · Cited by 37 · see citing works
Ma, X., Liu, C., Kong, X., Liu, J., Zhang, S., Liang, S., Luan, W., & Cao, X. (2021) · Science China Life Sciences · doi:10.1007/s11427-020-1891-8 · Cited by 34 · see citing works
tRNA derived small RNAs—Small players with big roles
George, S., Rafi, M., Aldarmaki, M., ElSiddig, M., Nuaimi, M. A., & Amiri, K. M. A. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.997780 · Cited by 34 · see citing works
Targeted sequencing reveals expanded genetic diversity of human transfer RNAs
Berg, M. D., Giguere, D. J., Dron, J. S., Lant, J. T., Genereaux, J. L., Liao, C., Wang, J., Robinson, J. F., Gloor, G. B., Hegele, R. A., et al. (2019) · RNA Biology · doi:10.1080/15476286.2019.1646079 · Cited by 33 · see citing works
A hypoxia-responsive tRNA-derived small RNA confers renal protection through RNA autophagy
Li, G., Sun, L., Xin, C., Tian, H., Kharel, P., Manning, A. C., O'Connor, C. L., Moore, H., Lei, S., Gokulnath, P., et al. (2025) · Science · doi:10.1126/science.adp5384 · Cited by 32 · see citing works
tRNAs and tRNA fragments as modulators of cardiac and skeletal muscle function
Liapi, E., van Bilsen, M., Verjans, R., & Schroen, B. L. M. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2019.03.012 · Cited by 32 · see citing works
Warren, J. M., Salinas‐Giegé, T., Hummel, G., Coots, N. L., Svendsen, J. M., Brown, K. C., Maréchal‐Drouard, L., & Sloan, D. B. (2020) · RNA Biology · doi:10.1080/15476286.2020.1792089 · Cited by 31 · see citing works
Effect of mRNA/tRNA mutations on translation speed: Implications for human diseases
Davyt, M., Bharti, N., & Ignatova, Z. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.105089 · Cited by 31 · see citing works
Coordination of transcription and processing of tRNA
Jarrous, N., Mani, D., & Ramanathan, A. S. K. (2021) · FEBS Journal · doi:10.1111/febs.15904 · Cited by 30 · see citing works
Deep sequencing of yeast and mouse tRNAs and tRNA fragments using OTTR
Gustafsson, H. T., Galan, C., Tianxiong, Y., Upton, H. E., Ferguson, L., Kaymak, E., Weng, Z., Collins, K., & Rando, O. J. (2025) · eLife · doi:10.7554/elife.77616 · Cited by 30 · see citing works
The cell stress response: extreme times call for post‐transcriptional measures
Pizzinga, M., Harvey, R. F., Garland, G. D., Mordue, R., Dezi, V., Ramakrishna, M., Sfakianos, A., Monti, M., Mulroney, T. E., Pöyry, T. A. A., et al. (2019) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1578 · Cited by 30 · see citing works
Zinnall, U., Milek, M., Minia, I., Vieira-Vieira, C. H., Müller, S., Mastrobuoni, G., Hazapis, O.-G., Del Giudice, S., Schwefel, D., Bley, N., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30322-7 · Cited by 30 · see citing works
Hayne, C. K., Butay, K. J. U., Stewart, Z. D., Krahn, J. M., Perera, L., Williams, J. G., Petrovitch, R. M., Deterding, L. J., Matera, A. G., Borgnia, M. J., et al. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-00991-z · Cited by 30 · see citing works
Mutation bias within oncogene families is related to proliferation-specific codon usage
Benisty, H., Weber, M. L., Hernandez‐Alias, X., Schaefer, M. H., & Serrano, L. G. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016119117 · Cited by 29 · see citing works
Gong, M., Deng, Y., Xiang, Y., & Ye, D. (2023) · Cell Communication and Signaling · doi:10.1186/s12964-023-01079-3 · Cited by 29 · see citing works
Gerstberger, S. C., Meyer, C., Benjamin, S., Rodriguez, J., Briskin, D., Bognanni, C., Bogardus, K. A., Steller, H., & Tuschl, T. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.09.067 · Cited by 29 · see citing works
Self-citationT-psi-C: user friendly database of tRNA sequences and structures
Sajek, M. P., Woźniak, T., Sprinzl, M., Jaruzelska, J., & Barciszewski, J. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz922 · Cited by 29 · see citing works
Gao, W. N. D., Gallardo-Dodd, C. J., & Kutter, C. (2021) · Genome Research · doi:10.1101/gr.275944.121 · Cited by 29 · see citing works
Alteration of the Premature tRNA Landscape by Gammaherpesvirus Infection
Tucker, J. M., Schaller, A. M., Willis, I. M., & Glaunsinger, B. A. (2020) · mBio · doi:10.1128/mbio.02664-20 · Cited by 28 · see citing works
Plant transfer RNA‐derived fragments: Biogenesis and functions
Ma, X., Liu, C., & Cao, X. (2021) · Journal of Integrative Plant Biology · doi:10.1111/jipb.13143 · Cited by 28 · see citing works
tRNA Biology in the Pathogenesis of Diabetes: Role of Genetic and Environmental Factors
Arroyo, M. N., Green, J. A., Cnop, M., & Igoillo‐Esteve, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020496 · Cited by 27 · see citing works
Revisiting tRNA chaperones: new players in an ancient game
Porat, J., Kothe, U., & Bayfield, M. A. (2021) · RNA · doi:10.1261/rna.078428.120 · Cited by 27 · see citing works
Structural basis of substrate recognition by human tRNA splicing endonuclease TSEN
Sekulovski, S., Sušac, L., Stelzl, L. S., Tampé, R., & Trowitzsch, S. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-00992-y · Cited by 27 · see citing works
Tao, E., Wang, Y., Tan, J., Chen, Y., Sun, T.-Y., Yu, H., Wang, H.-L., Liu, Q., Wang, Y.-Q., Fu, L., et al. (2025) · Nature Cancer · doi:10.1038/s43018-025-00977-4 · Cited by 26 · see citing works
Liu, Y.-T., Strugatsky, D., Liu, W., & Zhou, Z. H. (2021) · Nature Communications · doi:10.1038/s41467-021-25791-1 · Cited by 26 · see citing works
The multi‐faceted regulation of nuclear tRNA gene transcription
Hummel, G., Warren, J. M., & Maréchal‐Drouard, L. (2019) · IUBMB Life · doi:10.1002/iub.2097 · Cited by 26 · see citing works
The 3’tsRNAs are aminoacylated: Implications for their biogenesis
Liu, Z., Kim, H. K., Xu, J., Jing, Y., & Kay, M. A. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009675 · Cited by 25 · see citing works
Xu, H., Chen, W., Zheng, F., Tang, D., Dai, W., Huang, S., Zhang, C., Zeng, J., Wang, G., & Dai, Y. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.04.114 · Cited by 23 · see citing works
- Authors
- Gogakos, T., Brown, M., Garzia, A., Meyer, C., Hafner, M., & Tuschl, T.
- Affiliations
- Howard Hughes Medical Institute (US)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (US)
- Corresponding author
- Tuschl, Thomas
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2017-08
- Volume
- 20
- Issue
- 6
- Pages
- 1463-1475
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC5564215
- OpenAlex
- W2742715352
- Cited by
- 209
- References
- 48
- Citations by year
- 2026: 14 · 2025: 24 · 2024: 17 · 2023: 27 · 2022: 21 · 2021: 31 · 2020: 24 · 2019: 39 · 2018: 9 · 2017: 3
- FWCI
- 8.49
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- NIH (TRA R01CA159227)
- Weill Cornell/Rockefeller/Sloan-Kettering MD/PhD Program
- 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 modifications and cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- tRNA, tRNA processing, PAR-CLIP, pre-tRNA processing, RNA secondary structure, nucleotide modification, tRNA introns, tRNA expression, human cells
- MeSH terms
- Humans, RNA Processing, Post-Transcriptional, RNA, Transfer, Sequence Analysis, RNA, HEK293 Cells
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