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Characterizing Expression and Processing of Precursor and Mature Human tRNAs by Hydro-tRNAseq and PAR-CLIP
Open accessAbstract
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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“More recently, high-throughput tRNA-specific sequencing techniques have also been developed.”
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“A hydrolysis-based tRNA sequencing method further allowed detection of tRNA precursors (140).”
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Cites
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 1,733
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 1,215
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 1,173
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
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
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
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 872
tRNA biology charges to the frontPreprint
Phizicky, E. M., & Hopper, A. K. (2010) · Genes & Development · doi:10.1101/gad.1956510 · Cited by 764
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
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 513
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 504
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
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 476
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
Stefano, J. E. (1984) · Cell · doi:10.1016/0092-8674(84)90083-7 · Cited by 375
The genetic code : the molecular basis for genetic expression
Woese, C. R. (1967) · Harper & Row eBooks · Cited by 298
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 293
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 283
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 271
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
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 220
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 179
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
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
Mechanism of Eukaryotic RNA Polymerase III Transcription Termination
Nielsen, S., Yuzenkova, Y., & Zenkin, N. (2013) · Science · doi:10.1126/science.1237934 · Cited by 141
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 131
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
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 126
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
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 114
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
Self-citationDana, A., & Tuller, T. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002755 · Cited by 112
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
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
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 89
Self-citationArimbasseri, G. A., & Maraia, R. J. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.04.002 · Cited by 87
Arimbasseri, 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
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
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
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
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
Dana, A., & Tuller, T. (2014) · G3 Genes Genomes Genetics · doi:10.1534/g3.114.015099 · Cited by 55
Iben, J., & Maraia, R. J. (2012) · RNA · doi:10.1261/rna.032151.111 · Cited by 51
Conservation of the relative tRNA composition in healthy and cancerous tissues
Mahlab-Aviv, S., Tuller, T., & Linial, M. (2012) · RNA · doi:10.1261/rna.030775.111 · Cited by 48
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
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
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
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
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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
Behrens, A., Rodschinka, G., & Nedialkova, D. D. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.01.028 · Cited by 254
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Metadata
- 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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