RNA regulons: coordination of post-transcriptional events
Abstract
Recent findings demonstrate that multiple mRNAs are co-regulated by one or more sequence-specific RNA-binding proteins that orchestrate their splicing, export, stability, localization and translation. These and other observations have given rise to a model in which mRNAs that encode functionally related proteins are coordinately regulated during cell growth and differentiation as post-transcriptional RNA operons or regulons, through a ribonucleoprotein-driven mechanism. Here I describe several recently discovered examples of RNA operons in budding yeast, fruitfly and mammalian cells, and their potential importance in processes such as immune response, oxidative metabolism, stress response, circadian rhythms and disease. I close by considering the evolutionary wiring and rewiring of these combinatorial post-transcriptional gene-expression networks.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
RNA-binding proteins control many steps of co- and post-transcriptional gene expression, such as splicing, polyadenylation, capping, modification, export, localization, translation, and turnover.
“RNA-binding proteins (RBPs) regulate numerous aspects of co- and post-transcriptional gene expression, including RNA splicing, polyadenylation, capping, modification, export, localization, translation and turnover1,2.”
From A compendium of RNA-binding motifs for decoding gene regulation (2013) · cites this paper as [2]
Cites
Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., & Lötvall, J. O. (2007) · Nature Cell Biology · doi:10.1038/ncb1596 · Cited by 12,834 · see citing works
Coordinated Transcription of Key Pathways in the Mouse by the Circadian Clock
Panda, S., Antoch, M. P., Miller, B. H., Su, A. I., Schook, A. C., Straume, M., Schultz, P. G., Kay, S. A., Takahashi, J. S., & Hogenesch, J. B. (2002) · Cell · doi:10.1016/s0092-8674(02)00722-5 · Cited by 2,272 · see citing works
Transcriptional regulatory code of a eukaryotic genome
Harbison, C. T., Gordon, D. B., Lee, T. I., Rinaldi, N. J., MacIsaac, K. D., Danford, T., Hannett, N. M., Tagne, J., Reynolds, D. B., Yoo, J. Y., et al. (2004) · Nature · doi:10.1038/nature02800 · Cited by 2,116 · see citing works
Gene Regulation for Higher Cells: A Theory
Britten, R. J., & Davidson, E. H. (1969) · Science · doi:10.1126/science.165.3891.349 · Cited by 2,049 · see citing works
Stochastic mRNA Synthesis in Mammalian Cells
Raj, A., Peskin, C. S., Tranchina, D., Vargas, D. Y., & Tyagi, S. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040309 · Cited by 1,737 · see citing works
Noise in eukaryotic gene expression
Blake, W. J., Kærn, M., Cantor, C. R., & Collins, J. J. (2003) · Nature · doi:10.1038/nature01546 · Cited by 1,636 · see citing works
Extensive and divergent circadian gene expression in liver and heart
Storch, K.-F., Lipan, O., Leykin, I., Viswanathan, N., Davis, F. C., Wong, W. H., & Weitz, C. J. (2002) · Nature · doi:10.1038/nature744 · Cited by 1,509 · see citing works
Stress granules and processing bodies are dynamically linked sites of mRNP remodeling
Kedersha, N., Stoecklin, G., Ayodele, M. O., Yacono, P. W., Lykke‐Andersen, J., Fritzler, M. J., Scheuner, D. L., Kaufman, R. J., Golan, D. E., & Anderson, P. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200502088 · Cited by 1,494 · see citing works
Circadian rhythms from multiple oscillators: lessons from diverse organisms
Bell‐Pedersen, D., Cassone, V. M., Earnest, D. J., Golden, S. S., Hardin, P. E., Thomas, T. L., & Zoran, M. J. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1633 · Cited by 1,481 · see citing works
An extensive network of coupling among gene expression machines
Maniatis, T., & Reed, R. (2002) · Nature · doi:10.1038/416499a · Cited by 1,148 · see citing works
CLIP Identifies Nova-Regulated RNA Networks in the Brain
Ule, J., Jensen, K. B., Ruggiu, M., Mele, A., Ule, A., & Darnell, R. B. (2003) · Science · doi:10.1126/science.1090095 · Cited by 1,120 · see citing works
Brown, V., Jin, P., Ceman, S., Darnell, J. C., O'Donnell, W. T., Tenenbaum, S. A., Jin, X., Feng, Y., Wilkinson, K. D., Keene, J. D., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00568-2 · Cited by 1,109 · see citing works
Self-citationBrennan, C. M., & Steitz*, J. A. (2001) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000854 · Cited by 1,095 · see citing works
From Birth to Death: The Complex Lives of Eukaryotic mRNAs
Moore, M. J. (2005) · Science · doi:10.1126/science.1111443 · Cited by 1,003 · see citing works
Mammalian circadian biology: elucidating genome-wide levels of temporal organization
Lowrey, P. L., & Takahashi, J. S. (2004) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.5.061903.175925 · Cited by 976 · see citing works
The spliceosome deposits multiple proteins 20–24 nucleotides upstream of mRNA exon–exon junctions
Hir, H. L., Izaurralde, E., Maquat, L. E., & Moore, M. J. (2000) · The EMBO Journal · doi:10.1093/emboj/19.24.6860 · Cited by 970 · see citing works
A Unified Theory of Gene Expression
Orphanides, G., & Reinberg, D. (2002) · Cell · doi:10.1016/s0092-8674(02)00655-4 · Cited by 898 · see citing works
Taylor, G. A., Carballo, E., Lee, D. M., Lai, W. S., Thompson, M. J., Patel, D. D., Schenkman, D. I., Gilkeson, G. S., Broxmeyer, H. E., Haynes, B. F., et al. (1996) · Immunity · doi:10.1016/s1074-7613(00)80411-2 · Cited by 765 · see citing works
FMR1 Protein: Conserved RNP Family Domains and Selective RNA Binding
Ashley, C. T., Wilkinson, K. D., Reines, D., & Warren, S. T. (1993) · Science · doi:10.1126/science.7692601 · Cited by 741 · see citing works
Lai, W. S., Carballo, E., Strum, J. R., Kennington, E. A., Phillips, R. S., & Blackshear, P. J. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.6.4311 · Cited by 730 · see citing works
The evolutionary dynamics of eukaryotic gene order
Hurst, L. D., Pál, C., & Lercher, M. J. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1319 · Cited by 719 · see citing works
Precision and functional specificity in mRNA decay
Wang, Y., Liu, C. L., Storey, J. D., Tibshirani, R. J., Herschlag, D., & Brown, P. O. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.092538799 · Cited by 708 · see citing works
Human polymorphism at microRNAs and microRNA target sites
Saunders, M. A., Liang, H., & Li, W. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611347104 · Cited by 654 · see citing works
Gerber, A. P., Herschlag, D., & Brown, P. O. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020079 · Cited by 651 · see citing works
Gould, S. J., Booth, A. M., & Hildreth, J. E. K. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1831413100 · Cited by 638 · see citing works
A PUF family portrait: 3′UTR regulation as a way of life
Wickens, M., Bernstein, D. S., Kimble, J. E., & Parker, R. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(01)02616-6 · Cited by 615 · see citing works
Decay Rates of Human mRNAs: Correlation With Functional Characteristics and Sequence AttributesPreprint
Yang, E., van Nimwegen, E., Zavolan, M., Rajewsky, N., Schroeder, M., Magnasco, M., & Darnell, J. E., Jr. (2003) · Genome Research · doi:10.1101/gr.1272403 · Cited by 598 · see citing works
An RNA map predicting Nova-dependent splicing regulation
Ule, J., Stefani, G., Mele, A., Ruggiu, M., Wang, X., Taneri, B., Gaasterland, T., Blencowe, B. J., & Darnell, R. B. (2006) · Nature · doi:10.1038/nature05304 · Cited by 528 · see citing works
Phosphorylation of HuR by Chk2 Regulates SIRT1 Expression
Abdelmohsen, K., Pullmann, R., Lal, A., Kim, H. H., Galbán, S., Yang, X., Blethrow, J. D., Walker, M., Shubert, J., Gillespie, D. A., et al. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.01.011 · Cited by 527 · see citing works
Identification of a target RNA motif for RNA-binding protein HuR
de Silanes, I. L., Zhan, M., Lal, A., Yang, X., & Gorospe, M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306453101 · Cited by 502 · see citing works
Evidence for large domains of similarly expressed genes in the Drosophila genome
Spellman, P. T., & Rubin, G. M. (2002) · Journal of Biology · doi:10.1186/1475-4924-1-5 · Cited by 485 · see citing works
Casciola-Rosen, L. A., Rosen, A., Petri, M., & Schlissel, M. S. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.4.1624 · Cited by 483 · see citing works
Lykke‐Andersen, J., & Wagner, E. (2005) · Genes & Development · doi:10.1101/gad.1282305 · Cited by 482 · see citing works
RNA-MEDIATED NEUROMUSCULAR DISORDERS
Ranum, L. P. W., & Cooper, T. A. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.113014 · Cited by 472 · see citing works
Eukaryotic mRNPs May Represent Posttranscriptional Operons
Keene, J. D., & Tenenbaum, S. A. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00559-2 · Cited by 460 · see citing works
Self-citationRNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation
Mazan-Mamczarz, K., Galbán, S., de Silanes, I. L., Martindale, J. L., Atasoy, U., Keene, J. D., & Gorospe, M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1432104100 · Cited by 445 · see citing works
Self-citationCarballo, E., Lai, W. S., & Blackshear, P. J. (2000) · Blood · doi:10.1182/blood.v95.6.1891 · Cited by 442 · see citing works
Synexpression groups in eukaryotes
Niehrs, C., & Pollet, N. (1999) · Nature · doi:10.1038/990025 · Cited by 440 · see citing works
Dyskeratosis Congenita and Cancer in Mice Deficient in Ribosomal RNA Modification
Ruggero, D., Grisendi, S., Piazza, F., Rego, E. M., Mari, F., Rao, P. H., Cordon‐Cardo, C., & Pandolfi, P. P. (2003) · Science · doi:10.1126/science.1079447 · Cited by 435 · see citing works
A novel role for shuttling SR proteins in mRNA translationPreprint
Sanford, J. R., Gray, N. K., Beckmann, K., & Cáceres, J. F. (2004) · Genes & Development · doi:10.1101/gad.286404 · Cited by 407 · see citing works
Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays
Tenenbaum, S. A., Carson, C. C., Lager, P. J., & Keene, J. D. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.26.14085 · Cited by 397 · see citing works
Self-citationPathway to Totipotency: Lessons from Germ Cells
Seydoux, G., & Braun, R. E. (2006) · Cell · doi:10.1016/j.cell.2006.11.016 · Cited by 389 · see citing works
Puig, S., Askeland, E., & Thiele, D. J. (2005) · Cell · doi:10.1016/j.cell.2004.11.032 · Cited by 382 · see citing works
Interactions of CCCH Zinc Finger Proteins with mRNA
Lai, W. S., Carballo, E., Thorn, J. M., Kennington, E. A., & Blackshear, P. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001696200 · Cited by 378 · see citing works
Lam, L. T., Pickeral, O. K., Peng, A. C., Rosenwald, A., Hurt, E. M., Giltnane, J. M., Averett, L., Zhao, H. G., Davis, R. E., Sathyamoorthy, M., et al. (2001) · Genome biology · doi:10.1186/gb-2001-2-10-research0041 · Cited by 371 · see citing works
Eystathioy, T., Chan, E. K. L., Tenenbaum, S. A., Keene, J. D., Griffith, K. J., & Fritzler, M. J. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.01-11-0544 · Cited by 363 · see citing works
Self-citationLevine, T., Gao, F., King, P. H., Andrews, L. G., & Keene, J. D. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.6.3494 · Cited by 356 · see citing works
Self-citationGrigull, J., Mnaimneh, S., Pootoolal, J., Robinson, M. D., & Hughes, T. R. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.12.5534-5547.2004 · Cited by 342 · see citing works
Pan, Q., Shai, O., Misquitta, C., Zhang, W., Saltzman, A. L., Mohammad, N., Babak, T., Siu, H., Hughes, T. R., Morris, Q. D., et al. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.12.004 · Cited by 323 · see citing works
Why is Hu where? Shuttling of early-response-gene messenger RNA subsets
Keene, J. D. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.1.5 · Cited by 294 · see citing works
Self-citationeIF4E is a central node of an RNA regulon that governs cellular proliferation
Čuljković, B., Topisirović, I., Skrabanek, L. A., Ruiz‐Gutierrez, M., & Borden, K. L. B. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200607020 · Cited by 294 · see citing works
Form follows function: the genomic organization of cellular differentiationPreprint
Kosak, S. T., & Groudine, M. T. (2004) · Genes & Development · doi:10.1101/gad.1209304 · Cited by 294 · see citing works
Post-transcriptional control of gene expression: a genome-wide perspective
Mata, J., Marguerat, S., & Bähler, J. (2005) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2005.07.005 · Cited by 288 · see citing works
Gerber, A. P., Luschnig, S., Krasnow, M. A., Brown, P. O., & Herschlag, D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509260103 · Cited by 277 · see citing works
Bringing the role of mRNA decay in the control of gene expression into focus
Wilusz, C. J., & Wilusz, J. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.07.011 · Cited by 268 · see citing works
Post‐transcriptional regulation in cancer
Audic, Y., & Hartley, R. S. (2004) · Biology of the Cell · doi:10.1016/j.biolcel.2004.05.002 · Cited by 237 · see citing works
Epigenetic Activation of a Subset of mRNAs by eIF4E Explains Its Effects on Cell Proliferation
Mamane, Y., Petroulakis, E., Martineau, Y., Sato, T.-A., Larsson, O., Rajasekhar, V., & Sonenberg, N. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000242 · Cited by 237 · see citing works
Global analysis of stress-regulated mRNA turnover by using cDNA arrays
Fan, J., Yang, X., Wang, W., Wood, W. H., Becker, K. G., & Gorospe, M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.162212399 · Cited by 232 · see citing works
Antic, D., & Keene, J. D. (1997) · The American Journal of Human Genetics · doi:10.1086/514866 · Cited by 231 · see citing works
Self-citationKeene, J. D. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111145598 · Cited by 230 · see citing works
Self-citationIdentification and Functional Outcome of mRNAs Associated with RNA-Binding Protein TIA-1
de Silanes, I. L., Galbán, S., Martindale, J. L., Yang, X., Mazan-Mamczarz, K., Indig, F. E., Falco, G., Zhan, M., & Gorospe, M. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.21.9520-9531.2005 · Cited by 230 · see citing works
Paraneoplastic Syndromes Affecting the Nervous System
Darnell, R. B., & Posner, J. B. (2006) · Seminars in Oncology · doi:10.1053/j.seminoncol.2006.03.008 · Cited by 216 · see citing works
mRNA Stability and the Control of Gene Expression: Implications for Human Disease
Hollams, E. M., Giles, K. M., Thomson, A. M., & Leedman, P. J. (2002) · Neurochemical Research · doi:10.1023/a:1020992418511 · Cited by 210 · see citing works
Selfish operons and speciation by gene transfer
Lawrence, J. G. (1997) · Trends in Microbiology · doi:10.1016/s0966-842x(97)01110-4 · Cited by 210 · see citing works
Paraneoplastic Syndromes Affecting the Nervous System
Khasraw, M., & Khakoo, Y. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4377-0435-8.00101-3 · Cited by 203 · see citing works
Telomerase RNA level limits telomere maintenance in X-linked dyskeratosis congenitaPreprint
Wong, J. M. Y., & Collins, K. (2006) · Genes & Development · doi:10.1101/gad.1476206 · Cited by 201 · see citing works
Jain, R. G., Andrews, L. G., McGowan, K. M., Pekala, P. H., & Keene, J. D. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.2.954 · Cited by 199 · see citing works
Self-citationHieronymus, H., & Silver, P. A. (2003) · Nature Genetics · doi:10.1038/ng1080 · Cited by 194 · see citing works
García‐Rodríguez, L. J., Gay, A. C., & Pon, L. A. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200606054 · Cited by 186 · see citing works
Cheadle, C., Fan, J., Cho-Chung, Y. S., Werner, T., Ray, J., Do, L., Gorospe, M., & Becker, K. G. (2005) · BMC Genomics · doi:10.1186/1471-2164-6-75 · Cited by 183 · see citing works
On the sequencing of the human genome
Waterston, R., Lander, E. S., & Sulston, J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.042692499 · Cited by 180 · see citing works
Search for organising principles: understanding in systems biology
Mesarović, M., Keene, J. D., & Sreenath, S. N. (2004) · Systems Biology · doi:10.1049/sb:20045010 · Cited by 168 · see citing works
Self-citationCarrel, T. L., McWhorter, M. L., Workman, E., Zhang, H., Wolstencroft, E. C., Lorson, C. L., Bassell, G. J., Burghes, A. H. M., & Beattie, C. E. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1637-06.2006 · Cited by 165 · see citing works
Blumenthal, T. (2004) · Briefings in Functional Genomics and Proteomics · doi:10.1093/bfgp/3.3.199 · Cited by 163 · see citing works
A systems view of mRNP biologyPreprint
Hieronymus, H., & Silver, P. A. (2004) · Genes & Development · doi:10.1101/gad.1256904 · Cited by 157 · see citing works
Gao, F., Carson, C. C., Levine, T., & Keene, J. D. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.23.11207 · Cited by 156 · see citing works
Self-citationCPEB controls oocyte growth and follicle development in the mouse
Racki, W. J., & Richter, J. D. (2006) · Development · doi:10.1242/dev.02651 · Cited by 153 · see citing works
Local translation of classes of mRNAs that are targeted to neuronal dendrites
Eberwine, J. H., Miyashiro, K., Kacharmina, J. E., & Job, C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.121146698 · Cited by 148 · see citing works
Metazoan replication-dependent histone mRNAs: a distinct set of RNA polymerase II transcripts
Marzluff, W. F. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.04.010 · Cited by 148 · see citing works
Čuljković, B., Topisirović, I., & Borden, K. L. B. (2007) · Cell Cycle · doi:10.4161/cc.6.1.3688 · Cited by 147 · see citing works
Analysis of the V(D)J Recombination Efficiency at Lymphoid Chromosomal Translocation Breakpoints
Raghavan, S. C., Kirsch, I. R., & Lieber, M. R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m103797200 · Cited by 142 · see citing works
van der Walt, J. M., Noureddine, M., Kittappa, R., Hauser, M. A., Scott, W., Mckay, R. D. G., Zhang, F.-Y., Stajich, J., Fujiwara, K., Scott, B., et al. (2004) · American Journal of Human Genetics · doi:10.1086/421052 · Cited by 141 · see citing works
Raghavan, A., Robison, R. L., McNabb, J., Miller, C. R., Williams, D. A., & Bohjanen, P. R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m109511200 · Cited by 136 · see citing works
Yang, Q., Lishanski, A., Yang, W., Hatcher, S., Seet, H., & Gregg, J. P. (2003) · Genome Research · doi:10.1101/gr.997703 · Cited by 136 · see citing works
Lü, X., de la Peña, L., Barker, C. S., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3459 · Cited by 131 · see citing works
Metabolic Engineering in the -omics Era: Elucidating and Modulating Regulatory Networks
Vemuri, G. N., & Aristidou, A. A. (2005) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.69.2.197-216.2005 · Cited by 129 · see citing works
Post-transcriptional operons and regulons co-ordinating gene expression
Keene, J. D., & Lager, P. J. (2005) · Chromosome Research · doi:10.1007/s10577-005-0848-1 · Cited by 123 · see citing works
Self-citationHuR in the Mammalian Genotoxic Response: Post-Transcriptional Multitasking
Gorospe, M. (2003) · Cell Cycle · doi:10.4161/cc.2.5.491 · Cited by 121 · see citing works
The RNA-binding protein Musashi is required intrinsically to maintain stem cell identity
Siddall, N. A., McLaughlin, E. A., Marriner, N. L., & Hime, G. R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600906103 · Cited by 121 · see citing works
Positive patches and negative noodles: linking RNA processing to transcription?
Greenleaf, A. L. (1993) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(93)90016-g · Cited by 115 · see citing works
Intine, R. V. A., Tenenbaum, S. A., Sakulich, A. L., Keene, J. D., & Maraia, R. J. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00429-5 · Cited by 114 · see citing works
Self-citationA Nuclear Function of Hu Proteins as Neuron-specific Alternative RNA Processing Regulators
Zhu, H., Hasman, R. A., Barron, V. A., Luo, G., & Lou, H. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-02-0099 · Cited by 114 · see citing works
Lidder, P., Gutiérrez, R. A., Salomé, P. A., McClung, C. R., & Green, P. J. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.060368 · Cited by 111 · see citing works
The role of post-transcriptional regulation in chemokine gene expression in inflammation and allergy
Fan, J., Heller, N. M., Gorospe, M., Atasoy, U., & Stellato, C. (2005) · European Respiratory Journal · doi:10.1183/09031936.05.00120204 · Cited by 103 · see citing works
Guisbert, K. S. K., Duncan, K. E., Li, H., & Guthrie, C. (2005) · RNA · doi:10.1261/rna.7234205 · Cited by 97 · see citing works
Shared Strategies in Gene Organization among Prokaryotes and Eukaryotes
Lawrence, J. G. (2002) · Cell · doi:10.1016/s0092-8674(02)00900-5 · Cited by 97 · see citing works
Tap and NXT promote translation of unspliced mRNAPreprint
Jin, L., Guzik, B. W., Bor, Y.-C., Rekosh, D. M., & Hammarskjöld, M. (2003) · Genes & Development · doi:10.1101/gad.1155703 · Cited by 95 · see citing works
Verheesen, P., de Kluijver, A., van Koningsbruggen, S., et al. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi432 · Cited by 94 · see citing works
LARK activates posttranscriptional expression of an essential mammalian clock protein, PERIOD1
Kojima, S., Matsumoto, K., Hirose, M., Shimada, M., Nagano, M., Shigeyoshi, Y., Hoshino, S.-I., Ui‐Tei, K., Saigo, K., Green, C. B., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607567104 · Cited by 93 · see citing works
Benjamin, D., Schmidlin, M., Lu, M., Gross, B., & Moroni, C. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01099-06 · Cited by 91 · see citing works
Bor, Y.-C., Swartz, J. E., Morrison, A. A., et al. (2006) · Genes & Development · doi:10.1101/gad.1402306 · Cited by 91 · see citing works
Telomeres, Telomerase, and Human Disease
Artandi, S. E. (2006) · New England Journal of Medicine · doi:10.1056/nejmp068187 · Cited by 90 · see citing works
Gene Variants of VAMP8 and HNRPUL1 Are Associated With Early-Onset Myocardial Infarction
Shiffman, D., Rowland, C. M., Louie, J. Z., Luke, M. M., Bare, L. A., Bolonick, J. I., Young, B. A., Catanese, J. J., Stiggins, C. F., Pullinger, C. R., et al. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000226543.77214.e4 · Cited by 84 · see citing works
Immediate early response of the circadian polyA ribonuclease nocturnin to two extracellular stimuli
Garbarino‐Pico, E., Niu, S., Rollag, M. D., Strayer, C. A., Besharse, J. C., & Green, C. B. (2007) · RNA · doi:10.1261/rna.286507 · Cited by 82 · see citing works
Differential translation and fragile X syndrome
Vanderklish, P. W., & Edelman, G. M. (2005) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2005.00134.x · Cited by 81 · see citing works
Revealing Posttranscriptional Regulatory Elements Through Network-Level Conservation
Chan, C. S., Elemento, O., & Tavazoie, S. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0010069 · Cited by 79 · see citing works
Inada, M., & Guthrie, C. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307425100 · Cited by 79 · see citing works
Gama‐Carvalho, M., Barbosa‐Morais, N. L., Brodsky, A. S., Silver, P. A., & Carmo‐Fonseca, M. (2006) · Genome biology · doi:10.1186/gb-2006-7-11-r113 · Cited by 79 · see citing works
Duttagupta, R., Tian, B., Wilusz, C. J., Khounh, D. T., Soteropoulos, P., Ouyang, M., Dougherty, J. P., & Peltz, S. W. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.13.5499-5513.2005 · Cited by 79 · see citing works
Illegitimate transcription: Its use in the study of inherited disease
Kaplan, J., Kahn, A., & Chelly, J. (1992) · Human Mutation · doi:10.1002/humu.1380010502 · Cited by 76 · see citing works
Genome-wide analysis of mRNAs bound to the histone stem–loop binding protein
Townley-Tilson, W. H. D., Pendergrass, S. A., Marzluff, W. F., & Whitfield, M. L. (2006) · RNA · doi:10.1261/rna.76006 · Cited by 76 · see citing works
Cell-Specific RNA-Binding Proteins in Human Disease
Musunuru, K. (2003) · Trends in Cardiovascular Medicine · doi:10.1016/s1050-1738(03)00075-6 · Cited by 74 · see citing works
Moore, M. J., Schwartzfarb, E. M., Silver, P. A., & Yu, M. C. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.12.006 · Cited by 70 · see citing works
Regulation of local mRNA translation
Huang, Y., & Richter, J. D. (2004) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2004.03.002 · Cited by 69 · see citing works
Identification of mRNAs Associated with αCP2-Containing RNP Complexes
Waggoner, S. A., & Liebhaber, S. A. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.19.7055-7067.2003 · Cited by 69 · see citing works
Selective translation of mRNAs at synapses
Richter, J. D. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00318-5 · Cited by 68 · see citing works
Larsson, O. S., Perlman, D., Fan, D., Reilly, C., Peterson, M., Dahlgren, C., Liang, Z., Li, S., Polunovsky, V. A., Wahlestedt, C., et al. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl558 · Cited by 64 · see citing works
Similar gene expression profiles do not imply similar tissue functions
Yanai, I., Korbel, J. O., Boué, S., McWeeney, S. K., Peer Bork, B., & Lercher, M. J. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.01.006 · Cited by 59 · see citing works
Cooperative translational control of gene expression by Ras and Akt in cancer
Parsa, A. T., & Holland, E. C. (2004) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2004.10.009 · Cited by 57 · see citing works
The Cap-Dependent Translation Apparatus Integrates and Amplifies Cancer Pathways
Polunovsky, V. A., & Bitterman, P. B. (2006) · RNA Biology · doi:10.4161/rna.3.1.2718 · Cited by 57 · see citing works
Raghavan, A., Dhalla, M., Bakheet, T. M., Ogilvie, R. L., Louis, I. V.-S., Khabar, K. S. A., Williams, B. R. G., & Bohjanen, P. R. (2004) · Genomics · doi:10.1016/j.ygeno.2004.08.007 · Cited by 57 · see citing works
Robinson, D., Hammans, S. R., Read, S. P., et al. (2005) · Human Genetics · doi:10.1007/s00439-004-1235-2 · Cited by 56 · see citing works
Gene expression neighborhoods.
Oliver, B., Parisi, M. J., & Clark, D. (2002) · Journal of Biology · doi:10.1186/1475-4924-1-4 · Cited by 53 · see citing works
Eukaryotic operon-like transcription of functionally related genes in Drosophila
Ben‐Shahar, Y., Nannapaneni, K., Casavant, T. L., Scheetz, T. E., & Welsh, M. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609683104 · Cited by 53 · see citing works
Global Analysis of HuR-Regulated Gene Expression in Colon Cancer Systems of Reducing Complexity
de Silanes, I. L., Fan, J., Galbán, C. J., Spencer, R. G. S., Becker, K. G., & Gorospe, M. (2004) · Gene Expression · doi:10.3727/000000004783992215 · Cited by 41 · see citing works
Ocular motor indicators of executive dysfunction in fragile X and Turner syndromes
Lasker, A. G., Mazzocco, M. M. M., & Zee, D. S. (2006) · Brain and Cognition · doi:10.1016/j.bandc.2006.08.002 · Cited by 40 · see citing works
Rodrı́guez-Trelles, F., Tarrı́o, R., & Ayala, F. J. (2005) · BioEssays · doi:10.1002/bies.20241 · Cited by 35 · see citing works
Penalva, L. O. F., Burdick, M. D., Lin, S. M., Sutterlüty, H., & Keene, J. D. (2004) · Molecular Cancer · doi:10.1186/1476-4598-3-24 · Cited by 34 · see citing works
Self-citationEukaryotic Transcription: What Does It Mean for a Gene to Be ‘on’?
Golding, I., & Cox, E. C. (2006) · Current Biology · doi:10.1016/j.cub.2006.04.014 · Cited by 29 · see citing works
Coordinate stabilization of growth-regulatory transcripts in T cell malignancies
Louis, I. V.-S., MCNABB, J., Raghavan, A., Reilly, C., WILLIAMS, D., Bohjanen, K. A., & Bohjanen, P. R. (2005) · Genomics · doi:10.1016/j.ygeno.2005.04.013 · Cited by 28 · see citing works
Tenenbaum, S. A., Carson, C. C., Atasoy, U., & Keene, J. D. (2003) · Gene · doi:10.1016/s0378-1119(03)00661-9 · Cited by 27 · see citing works
Self-citationRNA-binding proteins and neural development: a matter of targets and complexes
Agnès, F., & Perron, M. (2004) · Neuroreport · doi:10.1097/00001756-200412030-00001 · Cited by 17 · see citing works
Chromosomal Organization: Mingling with the Neighbors
Aten, J. A., & Kanaar, R. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040155 · Cited by 17 · see citing works
En masse nascent transcription analysis to elucidate regulatory transcription factors
Fan, J. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj510 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
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
“To systematically seek possible roles for RBPs in mRNA stability, we identified cases in which there is a relationship between (1) the appearance of one or more strong motifs for an RBP in the 39 UTR, and (2) (anti-)correlation of the abundance of the transcript and the mRNA expression level of the RBP, over a diverse…”
HITS-CLIP yields genome-wide insights into brain alternative RNA processing
Licatalosi, D. D., Mele, A., Fak, J. J., Ule, J., Kayikci, M., Chi, S. W., Clark, T. A., Schweitzer, A. C., Blume, J. E., Wang, X., et al. (2008) · Nature · doi:10.1038/nature07488 · Cited by 1,352 · see citing works
“Genome-wide screens have been used to establish correlations between the action of RNABPs and biologic diversity6,7,26-30, but are unable to identify direct sites of RNA regulation.”
Genetic compensation: A phenomenon in search of mechanisms
El-Brolosy, M. A., & Stainier, D. Y. R. (2017) · PLOS Genetics · doi:10.1371/journal.pgen.1006780 · Cited by 829 · see citing works
Hogan, D. J., Riordan, D. P., Gerber, A. P., Herschlag, D., & Brown, P. O. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060255 · Cited by 609 · see citing works
Diverse molecular functions of Hu proteins
Hinman, M. N., & Lou, H. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8252-6 · Cited by 587 · see citing works
Protein–RNA interactions: new genomic technologies and perspectives
König, J., Zarnack, K., Luscombe, N. M., & Ule, J. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3141 · Cited by 555 · see citing works
mTOR coordinates protein synthesis, mitochondrial activity and proliferation
Morita, M., Gravel, S.-P., Hulea, L., Larsson, O., Pollak, M., St-Pierre, J., & Topisirovic, I. (2015) · Cell Cycle · doi:10.4161/15384101.2014.991572 · Cited by 552 · see citing works
Srikantan, S. (2012) · Frontiers in Bioscience · doi:10.2741/3921 · Cited by 353 · see citing works
RNA targets of wild-type and mutant FET family proteins
Hoell, J. I., Larsson, E., Runge, S., Nusbaum, J. D., Duggimpudi, S., Farazi, T. A., Hafner, M., Borkhardt, A., Sander, C., & Tuschl, T. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2163 · Cited by 350 · see citing works
Yap, K., Lim, Z. Q., Khandelia, P., Friedman, B., & Makeyev, E. V. (2012) · Genes & Development · doi:10.1101/gad.188037.112 · Cited by 286 · see citing works
Ji, Z., & Tian, B. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008419 · Cited by 264 · see citing works
miR-519 reduces cell proliferation by lowering RNA-binding protein HuR levels
Abdelmohsen, K., Srikantan, S., Kuwano, Y., & Gorospe, M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809376106 · Cited by 230 · see citing works
The regulation of mRNA stability in mammalian cells: 2.0
Wu, X., & Brewer, G. (2012) · Gene · doi:10.1016/j.gene.2012.03.021 · Cited by 239 · see citing works
An RNA toolbox for cancer immunotherapy
Pastor, F., Berraondo, P., Etxeberria, I., Frederick, J., Sahin, U., Gilboa, E., & Melero, I. (2018) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2018.132 · Cited by 229 · see citing works
The GAIT system: a gatekeeper of inflammatory gene expression
Mukhopadhyay, R., Jia, J., Arif, A., Ray, P. S., & Fox, P. L. (2009) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2009.03.004 · Cited by 216 · see citing works
Kundu, P., Fabian, M. R., Sonenberg, N., Bhattacharyya, S. N., & Filipowicz, W. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks148 · Cited by 180 · see citing works
Morris, A. R., Mukherjee, N., & Keene, J. D. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00155-08 · Cited by 155 · see citing works
Self-citationFatemi, S. H., Folsom, T. D., Kneeland, R. E., & Liesch, S. B. (2011) · The Anatomical Record · doi:10.1002/ar.21299 · Cited by 137 · see citing works
De Rubeis, S., & Bagni, C. (2010) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2009.09.013 · Cited by 126 · see citing works
Bronicki, L. M., & Jasmin, B. J. (2013) · RNA · doi:10.1261/rna.039164.113 · Cited by 126 · see citing works
Gene expression regulation in trypanosomatids
De Gaudenzi, J. G., Noé, G., Campo, V. A., Frasch, A. C., & Cassola, A. (2011) · Essays in Biochemistry · doi:10.1042/bse0510031 · Cited by 116 · see citing works
The REM phase of gene regulation
Hentze, M. W., & Preiss, T. (2010) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2010.05.009 · Cited by 115 · see citing works
The ribonome: a dominant force in co‐ordinating gene expression
Mansfield, K. D., & Keene, J. D. (2009) · Biology of the Cell · doi:10.1042/bc20080055 · Cited by 102 · see citing works
Self-citationKraushar, M. L., Thompson, K., Wijeratne, H. R. S., Viljetic, B., Sakers, K., Marson, J. W., Kontoyiannis, D. L., Buyske, S., Hart, R. P., & Rasin, M.-R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1408305111 · Cited by 98 · see citing works
Cenik, C., Chua, H. N., Zhang, H., Tarnawsky, S. P., Akef, A., Derti, A., Tasan, M., Moore, M. J., Palazzo, A. F., & Roth, F. P. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001366 · Cited by 87 · see citing works
Fatemi, S. H., & Folsom, T. D. (2011) · Molecular Autism · doi:10.1186/2040-2392-2-6 · Cited by 84 · see citing works
DeBoer, E. M., Azevedo, R., Vega, T. A., Brodkin, J., Akamatsu, W., Okano, H., Wagner, G. C., & Rasin, M.-R. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3703-13.2014 · Cited by 72 · see citing works
Calarco, J. A., Zhen, M., & Blencowe, B. J. (2011) · RNA · doi:10.1261/rna.2603911 · Cited by 72 · see citing works
Ratti, A., Fallini, C., Colombrita, C., Pascale, A., Laforenza, U., Quattrone, A., & Silani, V. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m706082200 · Cited by 66 · see citing works
Cellular oxygen sensing, signalling and how to survive translational arrest in hypoxia
Fähling, M. (2009) · Acta Physiologica · doi:10.1111/j.1748-1716.2008.01894.x · Cited by 57 · see citing works
RBM4: A multifunctional RNA-binding protein
Markus, M. A., & Morris, B. J. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.05.027 · Cited by 50 · see citing works
NF90 coordinately represses the senescence-associated secretory phenotype
Tominaga-Yamanaka, K., Abdelmohsen, K., Martindale, J. L., Yang, X., Taub, D. D., & Gorospe, M. (2012) · Aging · doi:10.18632/aging.100497 · Cited by 49 · see citing works
Stress Granules Contain Rbfox2 with Cell Cycle-related mRNAs
Park, C., Choi, S., Kim, Y.-E., Lee, S., Park, S.-H., Adelstein, R. S., Kawamoto, S., & Kim, K. K. (2017) · Scientific Reports · doi:10.1038/s41598-017-11651-w · Cited by 49 · see citing works
Post-transcriptional regulation of cytokine and growth factor signaling in cancer
Vlasova-St. Louis, I., & Bohjanen, P. R. (2017) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2016.11.004 · Cited by 47 · see citing works
- Authors
- Keene, J. D.
- Affiliations
- Duke University (US)
- Corresponding author
- Keene, Jack D.
- Venue
- Nature Reviews Genetics
- Published
- 2007-07
- Volume
- 8
- Issue
- 7
- Pages
- 533-543
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W2073424121
- Cited by
- 1,321
- References
- 134
- Citations by year
- 2026: 27 · 2025: 29 · 2024: 48 · 2023: 49 · 2022: 58 · 2021: 59 · 2020: 74 · 2019: 62 · 2018: 72 · 2017: 74 · 2016: 72 · 2015: 74 · 2014: 98 · 2013: 80 · 2012: 95
- FWCI
- 6.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Keywords
- RNA-binding proteins, post-transcriptional regulation, ribonucleoprotein complexes, mRNA splicing, mRNA export, mRNA stability, mRNA localization, translation (biology), cell differentiation, immune response, oxidative metabolism, stress response, circadian rhythm, gene expression networks, gene regulatory evolution
- MeSH terms
- Animals, Drosophila, Saccharomycetales, Gene Expression Regulation, Mammals, Models, Genetic, Operon, RNA, RNA Processing, Post-Transcriptional, RNA Splicing, Transcription, Genetic, Protein Biosynthesis, RNA-Binding Proteins, Regulon, Gene Regulatory Networks
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