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Extensive identification and analysis of conserved small ORFs in animals
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Abstract
BACKGROUND: There is increasing evidence that transcripts or transcript regions annotated as non-coding can harbor functional short open reading frames (sORFs). Loss-of-function experiments have identified essential developmental or physiological roles for a few of the encoded peptides (micropeptides), but genome-wide experimental or computational identification of functional sORFs remains challenging. RESULTS: Here, we expand our previously developed method and present results of an integrated computational pipeline for the identification of conserved sORFs in human, mouse, zebrafish, fruit fly, and the nematode C. elegans. Isolating specific conservation signatures indicative of purifying selection on amino acid (rather than nucleotide) sequence, we identify about 2,000 novel small ORFs located in the untranslated regions of canonical mRNAs or on transcripts annotated as non-coding. Predicted sORFs show stronger conservation signatures than those identified in previous studies and are sometimes conserved over large evolutionary distances. The encoded peptides have little homology to known proteins and are enriched in disordered regions and short linear interaction motifs. Published ribosome profiling data indicate translation of more than 100 novel sORFs, and mass spectrometry data provide evidence for more than 70 novel candidates. CONCLUSIONS: Taken together, we identify hundreds of previously unknown conserved sORFs in major model organisms. Our computational analyses and integration with experimental data show that these sORFs are expressed, often translated, and sometimes widely conserved, in some cases even between vertebrates and invertebrates. We thus provide an integrated resource of putatively functional micropeptides for functional validation in vivo.
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![Fig. 6 Experimental evidence supports translation of predicted sORFs and protein expression. a Translation is detected using the ORFscore method [10] on published ribosome profiling data. The Kolmogorov-Smirnov D-statistic is used to assess the performance of the dataset by comparing annotated sORFs to the negative control (dark gray). Length-matched non-conserved sORFs from non-coding transcriptome regions are included for comparison (light gray). ***P <0.001; **P <0.01; *P <0.05 (Mann-Whitney test). b Peptide expression of many predicted sORFs is confirmed by mining in house and published mass spectrometry datasets from cell lines and model organisms](/paper-figures/4c3a0fe071e945e4a5802c17b91bfc7c/extensive-identification-and-analysis-of-conserved-small-orfs-in-animals-figure-6.jpg)
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Cites
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566 · cited 2×
“[80], using mouse liver from Azimifar et al.”
MethodSelf-citationAndromeda: A Peptide Search Engine Integrated into the MaxQuant Environment
Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., & Mann, M. (2011) · Journal of Proteome Research · doi:10.1021/pr101065j · Cited by 5,520
Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites
Nielsen, H., Engelbrecht, J., Brunak, S., & von HEIJNE, G. (1997) · Protein Engineering Design and Selection · doi:10.1093/protein/10.1.1 · Cited by 5,343
The ENCODE Project Consortium (2007) · Nature · doi:10.1038/nature05874 · Cited by 5,223
Derrien, T., Johnson, R., Bussotti, G., Andrea Tanzer, A., Djebali, S., Tilgner, H., Guernec, G., Martin, D., Merkel, A., Knowles, D. G., et al. (2012) · Genome Research · doi:10.1101/gr.132159.111 · Cited by 5,135
Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals
Guttman, M., Amit, I., Garber, M., French, C., Lin, M. F., Feldser, D., Huarte, M., Zuk, O., Carey, B. W., Cassady, J. P., et al. (2009) · Nature · doi:10.1038/nature07672 · Cited by 4,098
Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes
Siepel, A., Bejerano, G., Pedersen, J. S., Hinrichs, A. S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L. W., Richards, S., et al. (2005) · Genome Research · doi:10.1101/gr.3715005 · Cited by 3,971 · cited 1×
“Finally, we extracted phastCons conservation scores [100] in 50 nt windows around start and stop codon (excluding introns but extending into flanking genomic sequence if necessary) and used the Euclidean distance of the phastCons profiles from the base-wise average over the positive set as third and fourth feature.”
MethodIntrinsically unstructured proteins and their functions
Dyson, H. J., & Wright, P. E. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1589 · Cited by 3,871
Cabili, M. N., Trapnell, C., Goff, L. A., Koziol, M. J., Tazón‐Vega, B., Regev, A., & Rinn, J. L. (2011) · Genes & Development · doi:10.1101/gad.17446611 · Cited by 3,551
The landscape of long noncoding RNAs in the human transcriptome
Iyer, M. K., Niknafs, Y. S., Malik, R., Singhal, U., Sahu, A., Hosono, Y., Barrette, T. R., Prensner, J. R., Evans, J. R., Zhao, S., et al. (2015) · Nature Genetics · doi:10.1038/ng.3192 · Cited by 2,738
lincRNAs: Genomics, Evolution, and Mechanisms
Ulitsky, I., & Bartel, D. P. (2013) · Cell · doi:10.1016/j.cell.2013.06.020 · Cited by 2,652
A Long Noncoding RNA Controls Muscle Differentiation by Functioning as a Competing Endogenous RNA
Cesana, M., Cacchiarelli, D., Legnini, I., Santini, T., Sthandier, O., Chinappi, M., Tramontano, A., & Bozzoni, I. (2011) · Cell · doi:10.1016/j.cell.2011.09.028 · Cited by 2,554
A draft map of the human proteome
Kim, M.-S., Pinto, S. M., Getnet, D., Nirujogi, R. S., Manda, S. S., Chaerkady, R., Madugundu, A. K., Kelkar, D. S., Isserlin, R., Jain, S., et al. (2014) · Nature · doi:10.1038/nature13302 · Cited by 2,198
Ingolia, N. T., Lareau, L. F., & Weissman, J. S. (2011) · Cell · doi:10.1016/j.cell.2011.10.002 · Cited by 2,187
Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples
Wagner, G. P., Kin, K., & Lynch, V. J. (2012) · Theory in Biosciences · doi:10.1007/s12064-012-0162-3 · Cited by 2,085
CPAT: Coding-Potential Assessment Tool using an alignment-free logistic regression model
Wang, L., Park, H. J., Dasari, S., Wang, S., Kocher, J., & Li, W. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt006 · Cited by 2,003
Dosztányi, Z., Csizmók, V., Tompa, P., & Simon, I. (2005) · Computer applications in the biosciences · doi:10.1093/bioinformatics/bti541 · Cited by 1,943
Mass-spectrometry-based draft of the human proteome
Wilhelm, M., Schlegl, J., Hahne, H., Gholami, A. M., Lieberenz, M., Savitski, M. M., Ziegler, E., Butzmann, L., Gessulat, S., Marx, H., et al. (2014) · Nature · doi:10.1038/nature13319 · Cited by 1,820
Sequencing and comparison of yeast species to identify genes and regulatory elements
Kellis, M., Patterson, N. J., Endrizzi, M. G., Birren, B. W., & Lander, E. S. (2003) · Nature · doi:10.1038/nature01644 · Cited by 1,751
A map of the cis-regulatory sequences in the mouse genome
Shen, Y., Yue, F., McCleary, D. F., Ye, Z., Edsall, L., Kuan, S., Wagner, U., Dixon, J., Lee, L., Lobanenkov, V. V., et al. (2012) · Nature · doi:10.1038/nature11243 · Cited by 1,361 · cited 1×
“For the expression analysis of sORF-containing transcripts we used RNA-seq data for 16 human tissues (Illumina Body Map), for 19 mouse tissues [103], for eight developmental stages of zebrafish [98], 24 developmental stages for fruit fly from modENCODE, and eight developmental stages in C.”
MethodGuttman, M., Garber, M., Levin, J. Z., Donaghey, J., Robinson, J., Adiconis, X., Fan, L., Koziol, M. J., Gnirke, A., Nusbaum, C., et al. (2010) · Nature Biotechnology · doi:10.1038/nbt.1633 · Cited by 1,253
A micropeptide encoded by a putative long noncoding RNA regulates muscle performance
Anderson, D. M., Anderson, K. M., Chang, C.-L., Makarewich, C. A., Nelson, B. R., McAnally, J. R., Kasaragod, P., Shelton, J. M., Liou, J., Bassel-Duby, R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.01.009 · Cited by 1,216
Conserved Function of lincRNAs in Vertebrate Embryonic Development despite Rapid Sequence Evolution
Ulitsky, I., Shkumatava, A., Jan, C. H., Sive, H. L., & Bartel, D. P. (2011) · Cell · doi:10.1016/j.cell.2011.11.055 · Cited by 1,197
PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regionsPreprint
Lin, M. F., Jungreis, I., & Kellis, M. (2010) · Nature Precedings · doi:10.1093/bioinformatics/btr209 · Cited by 1,031
The Xist lncRNA Exploits Three-Dimensional Genome Architecture to Spread Across the X Chromosome
Engreitz, J., Pandya‐Jones, A., McDonel, P. E., Shishkin, A., Sirokman, K., Surka, C., Kadri, S., Xing, J. C., Goren, A., Lander, E. S., et al. (2013) · Science · doi:10.1126/science.1237973 · Cited by 1,008
Integrative Analysis of the Caenorhabditis elegans Genome by the modENCODE Project
Gerstein, M., Lu, Z. J., Nostrand, E. L. V., Cheng, C., Arshinoff, B. I., Liu, T., Yip, K. Y.-L., Robilotto, R., Rechtsteiner, A., Ikegami, K., et al. (2010) · Science · doi:10.1126/science.1196914 · Cited by 973
Self-citationCalvo, S. E., Pagliarini, D. J., & Mootha, V. K. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810916106 · Cited by 914
Geiger, T., Wehner, A., Schaab, C., Cox, J., & Mann, M. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m111.014050 · Cited by 797
Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesisPreprint
Pauli, A., Valen, E., Lin, M. F., Garber, M. G., Vastenhouw, N. L., Levin, J. Z., Fan, L., Sandelin, A., Rinn, J. L., Regev, A., et al. (2011) · Genome Research · doi:10.1101/gr.133009.111 · Cited by 793
Ribosome Profiling Provides Evidence that Large Noncoding RNAs Do Not Encode Proteins
Guttman, M., Russell, P., Ingolia, N. T., Weissman, J. S., & Lander, E. S. (2013) · Cell · doi:10.1016/j.cell.2013.06.009 · Cited by 745
MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons
Ranwez, V., Harispe, S., Delsuc, F., & Douzery, E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022594 · Cited by 738
Peptidomic discovery of short open reading frame–encoded peptides in human cells
Slavoff, S. A., Mitchell, A. J., Schwaid, A. G., Cabili, M. N., Ma, J., Levin, J. Z., Karger, A., Budnik, B., Rinn, J. L., & Saghatelian, A. (2012) · Nature Chemical Biology · doi:10.1038/nchembio.1120 · Cited by 699
Hezroni, H., Koppstein, D., Schwartz, M. G., Avrutin, A., Bartel, D. P., & Ulitsky, I. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.04.023 · Cited by 677
Bazzini, A., Johnstone, T. G., Christiano, R., Mackowiak, S. D., Obermayer, B., Fleming, E. S., Vejnar, C. E., Lee, M. T., Rajewsky, N., Walther, T. C., et al. (2014) · The EMBO Journal · doi:10.1002/embj.201488411 · Cited by 675
Self-citationRibosome Profiling Reveals Pervasive Translation Outside of Annotated Protein-Coding Genes
Ingolia, N. T., Brar, G. A., Stern‐Ginossar, N., Harris, M. S., Talross, G. J. S., Jackson, S. E., Wills, M. R., & Weissman, J. S. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.045 · Cited by 670
Proto-genes and de novo gene birth
Carvunis, A.-R., Rolland, T., Wapinski, I., Calderwood, M. A., Yildirim, M. A., Simonis, N., Charloteaux, B., Hidalgo, C. A., Barbette, J., Santhanam, B., et al. (2012) · Nature · doi:10.1038/nature11184 · Cited by 669
OpenMS – An open-source software framework for mass spectrometry
Sturm, M., Bertsch, A., Gröpl, C., Hildebrandt, A., Hussong, R., Lange, E., Pfeifer, N., Schulz-Trieglaff, O. B., Zerck, A., Reinert, K., et al. (2008) · BMC Bioinformatics · doi:10.1186/1471-2105-9-163 · Cited by 656
RNA 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
Toddler: An Embryonic Signal That Promotes Cell Movement via Apelin Receptors
Pauli, A., Norris, M. L., Valen, E., Chew, G.-L., Gagnon, J. A., Zimmerman, S., Mitchell, A., Ma, J., Dubrulle, J., Reyon, D., et al. (2014) · Science · doi:10.1126/science.1248636 · Cited by 622
Global mapping of translation initiation sites in mammalian cells at single-nucleotide resolution
Lee, S., Liu, B., Lee, S., Huang, S., Shen, B., & Qian, S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1207846109 · Cited by 610
Finding the genes in genomic DNA
Burge, C. B., & Karlin, S. (1998) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(98)80069-9 · Cited by 586
Emerging evidence for functional peptides encoded by short open reading frames
Andrews, S. J., & Rothnagel, J. A. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3520 · Cited by 569
Long non-coding RNAs as a source of new peptides
Ruiz‐Orera, J., Messeguer, X., Subirana, J. A., & Albà, M. M. (2014) · eLife · doi:10.7554/elife.03523 · Cited by 560
Differentiating Protein-Coding and Noncoding RNA: Challenges and Ambiguities
Dinger, M. E., Pang, K. C., Mercer, T. R., & Mattick, J. S. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000176 · Cited by 538
A Million Peptide Motifs for the Molecular Biologist
Tompa, P., Davey, N. E., Gibson, T. J., & Babu, M. M. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.05.032 · Cited by 515
Pseudogenes: Pseudo-functional or key regulators in health and disease?
Pink, R. C., Wicks, K., Caley, D. P., Punch, E. K., Jacobs, L. A., & Carter, D. R. F. (2011) · RNA · doi:10.1261/rna.2658311 · Cited by 459
Chick, J. M., Kolippakkam, D. N., Nusinow, D. P., Zhai, B., Rad, R., Huttlin, E. L., & Gygi, S. P. (2015) · Nature Biotechnology · doi:10.1038/nbt.3267 · Cited by 435
Three classes of C2H2 zinc finger proteins
Iuchi, S. (2001) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000885 · Cited by 415
Long noncoding RNAs are rarely translated in two human cell linesPreprint
Bánfai, B., Jia, H., Khatun, J., Wood, E., Risk, B., Gundling, W. E., Kundaje, A., Gunawardena, H. P., Yu, Y., Xie, L., et al. (2012) · Genome Research · doi:10.1101/gr.134767.111 · Cited by 399
Ribosome profiling reveals pervasive and regulated stop codon readthrough in Drosophila melanogaster
Dunn, J. G., Foo, C. K., Belletier, N. G., Gavis, E. R., & Weissman, J. S. (2013) · eLife · doi:10.7554/elife.01179 · Cited by 392
Extensive localization of long noncoding RNAs to the cytosol and mono- and polyribosomal complexes
van Heesch, S., van Iterson, M., Jacobi, J., Boymans, S., Essers, P., de Bruijn, E., Hao, W., MacInnes, A. W., Cuppen, E. P. J. G., & Simonis, M. (2014) · Genome biology · doi:10.1186/gb-2014-15-1-r6 · Cited by 375
Conserved Regulation of Cardiac Calcium Uptake by Peptides Encoded in Small Open Reading Frames
Magny, E. G., Pueyo, J. I., Pearl, F. M. G., Céspedes, M. A., Niven, J. E., Bishop, S. A., & Couso, J. P. (2013) · Science · doi:10.1126/science.1238802 · Cited by 368
Peptides Encoded by Short ORFs Control Development and Define a New Eukaryotic Gene Family
Galindo, M. I., Pueyo, J. I., Fouix, S., Bishop, S. A., & Couso, J. P. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050106 · Cited by 366
The GENCODE pseudogene resource
Pei, B., Sisu, C., Frankish, A., Howald, C., Habegger, L., Mu, X. J., Harte, R., Balasubramanian, S., Andrea Tanzer, A., Diekhans, M., et al. (2012) · Genome biology · doi:10.1186/gb-2012-13-9-r51 · Cited by 356
Considerations when investigating lncRNA function in vivo
Bassett, A. R., Akhtar, A., Barlow, D. P., Bird, A. P., Brockdorff, N., Duboule, D., Ephrussi, A., Ferguson‐Smith, A. C., Gingeras, T., Haerty, W., et al. (2014) · eLife · doi:10.7554/elife.03058 · Cited by 356
Small Peptides Switch the Transcriptional Activity of Shavenbaby During Drosophila Embryogenesis
Kondo, T., Plaza, S., Zanet, J., Benrabah, E., Valenti, P., Hashimoto, Y., Kobayashi, S., Payre, F., & Kageyama, Y. (2010) · Science · doi:10.1126/science.1188158 · Cited by 348
Extensive translation of small Open Reading Frames revealed by Poly-Ribo-Seq
Aspden, J. L., Eyre‐Walker, Y. C., Phillips, R. J., Amin, U., Mumtaz, M. A., Brocard, M., & Couso, J. P. (2014) · eLife · doi:10.7554/elife.03528 · Cited by 341
The eukaryotic linear motif resource ELM: 10 years and counting
Dinkel, H., Roey, K. V., Michael, S., Davey, N. E., Weatheritt, R. J., Born, D., Speck, T., Krüger, D., Grebnev, G., Kubań, M., et al. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1047 · Cited by 301
Ribosome profiling reveals resemblance between long non-coding RNAs and 5′ leaders of coding RNAs
Chew, G.-L., Pauli, A., Rinn, J. L., Regev, A., Schier, A. F., & Valen, E. (2013) · Development · doi:10.1242/dev.098343 · Cited by 275
Small peptide regulators of actin-based cell morphogenesis encoded by a polycistronic mRNA
Kondo, T., Hashimoto, Y. K., Kato, K., Inagaki, S., Hayashi, S., & Kageyama, Y. (2007) · Nature Cell Biology · doi:10.1038/ncb1595 · Cited by 260
Quantitative profiling of initiating ribosomes in vivo
Gao, X., Wan, J., Liu, B., Ma, M., Shen, B., & Qian, S. (2014) · Nature Methods · doi:10.1038/nmeth.3208 · Cited by 244
Evidence of efficient stop codon readthrough in four mammalian genes
Loughran, G., Chou, M.-Y., Ivanov, I. P., Jungreis, I., Kellis, M., Kiran, A. M., Baranov, P. V., & Atkins, J. F. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku608 · Cited by 236
The Abundance of Short Proteins in the Mammalian Proteome
Frith, M. C., Forrest, A. R. R., Nourbakhsh, E., Pang, K. C., Kai, C., Kawai, J., Carninci, P., Hayashizaki, Y., Bailey, T. L., & Grimmond, S. M. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020052 · Cited by 234
Evidence of abundant stop codon readthrough in Drosophila and other metazoaPreprint
Jungreis, I., Lin, M. F., Spokony, R. F., Chan, C. S., Negre, N., Victorsen, A., White, K. P., & Kellis, M. (2011) · Genome Research · doi:10.1101/gr.119974.110 · Cited by 232
Expression of distinct RNAs from 3′ untranslated regions
Mercer, T. R., Wilhelm, D., Dinger, M. E., Soldà, G., Korbie, D. J., Glazov, E. A., Truong, V., Schwenke, M., Simons, C., Matthaei, K. I., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1158 · Cited by 225
Vanderperre, B., Lucier, J., Bissonnette, C., Motard, J., Tremblay, G., Vanderperre, S., Wisztorski, M., Salzet, M., Boisvert, F., & Roucou, X. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070698 · Cited by 223
Functional genomics of genes with small open reading frames (sORFs) in S. cerevisiaePreprint
Kastenmayer, J. P., Ni, L., Chu, A. M., Kitchen, L. E., Au, W.-C., Yang, H., Carter, C. D., Wheeler, D. L., Davis, R. W., Boeke, J. D., et al. (2006) · Genome Research · doi:10.1101/gr.4355406 · Cited by 220
Drosophila Pgc protein inhibits P-TEFb recruitment to chromatin in primordial germ cells
Hanyu‐Nakamura, K., Sonobe-Nojima, H., Tanigawa, A., Lasko, P. F., & Nakamura, A. (2008) · Nature · doi:10.1038/nature06498 · Cited by 213
Identification and Properties of 1,119 Candidate LincRNA Loci in the Drosophila melanogaster Genome
Young, R. S., Marques, A. C., Tibbit, C., Haerty, W., Bassett, A. R., Liu, J., & Ponting, C. P. (2012) · Genome Biology and Evolution · doi:10.1093/gbe/evs020 · Cited by 203
A 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 202
Discovery of Human sORF-Encoded Polypeptides (SEPs) in Cell Lines and Tissue
Ma, J., Ward, C., Jungreis, I., Slavoff, S. A., Schwaid, A. G., Neveu, J. M., Budnik, B., Kellis, M., & Saghatelian, A. (2014) · Journal of Proteome Research · doi:10.1021/pr401280w · Cited by 193
Savitski, M. M., Nielsen, M. L., & Zubarev, R. A. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.t500034-mcp200 · Cited by 188
The SILAC Fly Allows for Accurate Protein Quantification in Vivo*
Sury, M., Chen, J.-X., & Selbach, M. (2010) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.000323 · Cited by 185
Self-citationDENR–MCT-1 promotes translation re-initiation downstream of uORFs to control tissue growth
Schleich, S., Straßburger, K., Janiesch, P. C., Koledachkina, T., Miller, K. K., Haneke, K., Cheng, Y.-S., Küchler, K., Stoecklin, G., Duncan, K. E., et al. (2014) · Nature · doi:10.1038/nature13401 · Cited by 178
Revisiting the protein-coding gene catalog of Drosophila melanogaster using 12 fly genomes.Preprint
Lin, M. F., Carlson, J., Crosby, M., Matthews, B., Yu, C., Park, S., Wan, K. H., Schroeder, A., Gramates, L., Pierre, S. E. S., et al. (2007) · Genome Research · doi:10.1101/gr.6679507 · Cited by 174
Cell-Type-Resolved Quantitative Proteomics of Murine Liver
Azimifar, S. B., Nagaraj, N., Cox, J., & Mann, M. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.11.002 · Cited by 173
Smith, J. E., Alvarez‐Dominguez, J. R., Kline, N., Huynh, N. J., Geisler, S., Hu, W., Coller, J., & Baker, K. E. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.05.023 · Cited by 170
Hundreds of putatively functional small open reading frames in Drosophila
Ladoukakis, E. D., Pereira, V., Magny, E. G., Eyre‐Walker, A., & Couso, J. P. (2011) · Genome biology · doi:10.1186/gb-2011-12-11-r118 · Cited by 168
Savard, J., Marques‐Souza, H., Aranda, M., & Tautz, D. (2006) · Cell · doi:10.1016/j.cell.2006.05.053 · Cited by 160
Defining a minimal cell: essentiality of small ORFs and ncRNAs in a genome‐reduced bacterium
Lluch‐Senar, M., Delgado, J., Chen, W., Lloréns‐Rico, V., O’Reilly, F. J., Wodke, J. A. H., Unal, E. B., Yus, E., Martínez, S., Nichols, R. J., et al. (2015) · Molecular Systems Biology · doi:10.15252/msb.20145558 · Cited by 143
Putatively Noncoding Transcripts Show Extensive Association with Ribosomes
Wilson, B. A., & Masel, J. (2011) · Genome Biology and Evolution · doi:10.1093/gbe/evr099 · Cited by 134
Conservation of mRNA and Protein Expression during Development of C. elegans
Grün, D., Kirchner, M., Thierfelder, N., Stoeckius, M., Selbach, M., & Rajewsky, N. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.01.001 · Cited by 120
Self-citationRibosome Profiling Reveals a Cell-Type-Specific Translational Landscape in Brain Tumors
Gonzalez, C., Sims, J. S., Hornstein, N., Mela, A., Garcia, F., Lei, L., Gass, D. A., Amendolara, B., Bruce, J. N., Canoll, P., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0084-14.2014 · Cited by 116
Kellis, M., Patterson, N. J., Birren, B. W., Berger, B., & Lander, E. S. (2004) · Journal of Computational Biology · doi:10.1089/1066527041410319 · Cited by 113
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Metadata
- Authors
- Mackowiak, S. D., Zauber, H., Bielow, C., Thiel, D., Kutz, K., Calviello, L., Mastrobuoni, G., Rajewsky, N., Kempa, S., Selbach, M., & Obermayer, B.
- Affiliations
- Max Delbrück Center (DE)
- Corresponding author
- Obermayer, Benedikt
- ORCID
- Venue
- Genome Biology
- Published
- 2015-09-14
- Volume
- 16
- Issue
- 1
- Pages
- 179-179
- ISSN
- 1465-6906 (ISSN-L)
- 1474-760X
- PMC
- PMC4568590
- OpenAlex
- W2154350719
- Cited by
- 227
- References
- 104
- Citations by year
- 2026: 8 · 2025: 21 · 2024: 23 · 2023: 29 · 2022: 20 · 2021: 26 · 2020: 21 · 2019: 11 · 2018: 27 · 2017: 25 · 2016: 10 · 2015: 6
- FWCI
- 9.85
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Genome biology (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- small open reading frames, micropeptides, purifying selection, untranslated regions, non-coding transcripts, protein disorder, ribosome profiling, translation (biology), evolutionary conservation, model organisms
- MeSH terms
- Amino Acid Sequence, Animals, Exons, Humans, Peptides, Protein Biosynthesis, Open Reading Frames, Sequence Alignment, Conserved Sequence, Codon, Terminator, 3' Untranslated Regions, Amino Acid Motifs, Mice
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