RIOK2 phosphorylation by RSK promotes synthesis of the human small ribosomal subunit
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Abstract
Ribosome biogenesis lies at the nexus of various signaling pathways coordinating protein synthesis with cell growth and proliferation. This process is regulated by well-described transcriptional mechanisms, but a growing body of evidence indicates that other levels of regulation exist. Here we show that the Ras/mitogen-activated protein kinase (MAPK) pathway stimulates post-transcriptional stages of human ribosome synthesis. We identify RIOK2, a pre-40S particle assembly factor, as a new target of the MAPK-activated kinase RSK. RIOK2 phosphorylation by RSK stimulates cytoplasmic maturation of late pre-40S particles, which is required for optimal protein synthesis and cell proliferation. RIOK2 phosphorylation facilitates its release from pre-40S particles and its nuclear re-import, prior to completion of small ribosomal subunits. Our results bring a detailed mechanistic link between the Ras/MAPK pathway and the maturation of human pre-40S particles, which opens a hitherto poorly explored area of ribosome biogenesis.
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TOR signaling in growth and metabolism
Wullschleger, S., Loewith, R., & Hall, M. N. (2006) · Cell · doi:10.1016/j.cell.2006.01.016 · Cited by 5,787 · see citing works
Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases
Cargnello, M., & Roux, P. P. (2011) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00031-10 · Cited by 3,274 · see citing works
Self-citationmTOR at the nexus of nutrition, growth, ageing and disease
Liu, G. Y., & Sabatini, D. M. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0199-y · Cited by 2,737 · see citing works
The economics of ribosome biosynthesis in yeast
Warner, J. R. (1999) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01460-7 · Cited by 1,933 · see citing works
SUnSET, a nonradioactive method to monitor protein synthesis
Schmidt, E. K., Clavarino, G., Ceppi, M., & Pierre, P. (2009) · Nature Methods · doi:10.1038/nmeth.1314 · Cited by 1,706 · see citing works
Ribosome Biogenesis in the Yeast Saccharomyces cerevisiae
Woolford, J. L., & Baserga, S. J. (2013) · Genetics · doi:10.1534/genetics.113.153197 · Cited by 761 · see citing works
Roux, P. P., Shahbazian, D., Vu, H., Holz, M. K., Cohen, M. S., Taunton, J., Sonenberg, N., & Blenis, J. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700906200 · Cited by 749 · see citing works
Self-citationRapamycin selectively represses translation of the "polypyrimidine tract" mRNA family.
Jefferies, H. B. J., Reinhard, C., Kozma, S. C., & Thomas, G. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.10.4441 · Cited by 623 · see citing works
An overview of pre‐ribosomal RNA processing in eukaryotes
Henras, A. K., Plisson‐Chastang, C., O’Donohue, M.-F., Chakraborty, A., & Gleizes, P. (2014) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1269 · Cited by 597 · see citing works
Self-citationMarguerat, S., Schmidt, A., Codlin, S., Chen, W., Aebersold, R., & Bähler, J. (2012) · Cell · doi:10.1016/j.cell.2012.09.019 · Cited by 571 · see citing works
Life on a planet of its own: Regulation of RNA polymerase I transcription in the nucleolus
Grummt, I. (2003) · Genes & Development · doi:10.1101/gad.1098503r · Cited by 540 · see citing works
Tafforeau, L., Zorbas, C., Langhendries, J.-L., Mullineux, S.-T., Stamatopoulou, V., Mullier, R., Wacheul, L., & Lafontaine, D. L. J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.08.011 · Cited by 492 · see citing works
Kressler, D., Hurt, E., & Baßler, J. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2009.10.009 · Cited by 492 · see citing works
Ribosomopathies: There’s strength in numbers
Mills, E. W., & Green, R. (2017) · Science · doi:10.1126/science.aan2755 · Cited by 424 · see citing works
Regulation and function of the RSK family of protein kinases
Roméo, Y., Zhang, X., & Roux, P. P. (2011) · Biochemical Journal · doi:10.1042/bj20110289 · Cited by 379 · see citing works
Self-citationSignaling Pathways Involved in the Regulation of mRNA Translation
Roux, P. P., & Topisirović, I. (2018) · Molecular and Cellular Biology · doi:10.1128/mcb.00070-18 · Cited by 314 · see citing works
Self-citationRibosomal protein S6 kinase activity controls the ribosome biogenesis transcriptional program
Chauvin, C., Koka, V., Nouschi, A., Mieulet, V., Hoareau‐Aveilla, C., Dreazen, A., Cagnard, N., Carpentier, W., Kiss, T., Meyuhas, O., et al. (2013) · Oncogene · doi:10.1038/onc.2012.606 · Cited by 279 · see citing works
Zhao, J., Yuan, X., Frödin, M., & Grummt, I. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00036-4 · Cited by 259 · see citing works
Stefanovsky, V. Y., Pelletier, G., Hannan, R. D., Gagnon-Kugler, T., Rothblum, L. I., & Moss, T. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00384-7 · Cited by 242 · see citing works
Stefanovsky, V. Y., Langlois, F., Gagnon-Kugler, T., Rothblum, L. I., & Moss, T. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.01.023 · Cited by 220 · see citing works
Like Attracts Like: Getting RNA Processing Together in the Nucleus
Lewis, J., & Tollervey, D. W. (2000) · Science · doi:10.1126/science.288.5470.1385 · Cited by 220 · see citing works
Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit
Schäfer, T., Maco, B., Petfalski, E., Tollervey, D. W., Böttcher, B., Aebi, U., & Hurt, E. (2006) · Nature · doi:10.1038/nature04840 · Cited by 220 · see citing works
Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits
O’Donohue, M.-F., Choesmel, V., Faubladier, M., Fichant, G. A., & Gleizes, P. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201005117 · Cited by 219 · see citing works
Uncovering the assembly pathway of human ribosomes and its emerging links to disease
Bohnsack, K. E., & Bohnsack, M. T. (2019) · The EMBO Journal · doi:10.15252/embj.2018100278 · Cited by 217 · see citing works
Wild, T., Horváth, P., Wyler, E., Widmann, B., Badertscher, L., Zemp, I., Kozak, K., Csúcs, G., Lund, E., & Kutay, U. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000522 · Cited by 203 · see citing works
Powering through ribosome assembly
Strunk, B. S., & Karbstein, K. (2009) · RNA · doi:10.1261/rna.1792109 · Cited by 191 · see citing works
Herbert, T. P., Tee, A. R., & Proud, C. G. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110367200 · Cited by 181 · see citing works
Rouquette, J., Choesmel, V., & Gleizes, P. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600752 · Cited by 180 · see citing works
Marker-free coselection for CRISPR-driven genome editing in human cells
Agudelo, D., Duringer, A., Bozoyan, L., Huard, C., Carter, S., Loehr, J., Synodinou, D., Drouin, M., Salsman, J., Dellaire, G., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4265 · Cited by 174 · see citing works
A Puzzle of Life: Crafting Ribosomal Subunits
Kressler, D., Hurt, E., & Baßler, J. (2017) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2017.05.005 · Cited by 165 · see citing works
Regulation and Interaction of pp90 Isoforms with Mitogen-activated Protein Kinases
Zhao, Y., Bjørbæk, C., & Moller, D. E. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.47.29773 · Cited by 158 · see citing works
Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2
Zemp, I., Wild, T., O’Donohue, M.-F., Wandrey, F., Widmann, B., Gleizes, P., & Kutay, U. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200904048 · Cited by 155 · see citing works
Visualizing late states of human 40S ribosomal subunit maturation
Ameismeier, M., Cheng, J., Berninghausen, O., & Beckmann, R. (2018) · Nature · doi:10.1038/s41586-018-0193-0 · Cited by 149 · see citing works
Regulation of Ribosomal Protein mRNA Content and Translation in Growth-Stimulated Mouse Fibroblasts
Geyer, P., Meyuhas, O., Perry, R. P., & Johnson, L. F. (1982) · Molecular and Cellular Biology · doi:10.1128/mcb.2.6.685-693.1982 · Cited by 144 · see citing works
Dufresne, S. D., Bjørbæk, C., El-Haschimi, K., Zhao, Y., Aschenbach, W. G., Moller, D. E., & Goodyear, L. J. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.1.81-87.2001 · Cited by 139 · see citing works
Vanrobays, E., Gélugne, J., Gleizes, P., & Caizergues‐Ferrer, M. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.6.2083-2095.2003 · Cited by 139 · see citing works
ATPase-dependent role of the atypical kinase Rio2 on the evolving pre-40S ribosomal subunit
Ferreira-Cerca, S., Sagar, V., Schäfer, T., Diop, M., Wesseling, A.-M., Lu, H., Chai, E., Hurt, E., & LaRonde-LeBlanc, N. A. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2403 · Cited by 137 · see citing works
Read, R., Fenton, T., Gomez, G., Wykosky, J., Vandenberg, S., Babic, I., Iwanami, A., Yang, H.-J., Cavenee, W., Mischel, P., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003253 · Cited by 128 · see citing works
LaRonde-LeBlanc, N. A., & Wlodawer, A. (2005) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2005.07.037 · Cited by 125 · see citing works
Pre-Ribosomal RNA Processing in Human Cells: From Mechanisms to Congenital Diseases
Aubert, M., O’Donohue, M.-F., Lebaron, S., & Gleizes, P. (2018) · Biomolecules · doi:10.3390/biom8040123 · Cited by 122 · see citing works
Diverse Regulators of Human Ribosome Biogenesis Discovered by Changes in Nucleolar Number
Farley‐Barnes, K. I., McCann, K. L., Ogawa, L. M., Merkel, J., Surovtseva, Y. V., & Baserga, S. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.01.056 · Cited by 115 · see citing works
The mitogen‐activated protein (MAP) kinase ERK induces tRNA synthesis by phosphorylating TFIIIB
Felton-Edkins, Z. A., Fairley, J. A., Graham, E. L., Johnston, I. M., White, R. J., & Scott, P. H. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg240 · Cited by 114 · see citing works
Defining the role of the RSK isoforms in cancer
Houlès, T., & Roux, P. P. (2017) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2017.04.016 · Cited by 113 · see citing works
Self-citationHerbert, T. P., Kilhams, G. R., Batty, I. H., & Proud, C. G. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.15.11249 · Cited by 107 · see citing works
Widmann, B., Wandrey, F., Badertscher, L., Wyler, E., Pfannstiel, J., Zemp, I., & Kutay, U. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-07-0639 · Cited by 106 · see citing works
mTOR signaling regulates the processing of pre-rRNA in human cells
Iadevaia, V., Zhang, Z., Jan, E., & Proud, C. G. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1040 · Cited by 102 · see citing works
Signal Transduction in Ribosome Biogenesis: A Recipe to Avoid Disaster
Piazzi, M., Bavelloni, A., Gallo, A., Faenza, I., & Blalock, W. L. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20112718 · Cited by 102 · see citing works
Badertscher, L., Wild, T., Montellese, C., Alexander, L. T., Bammert, L., Sárazová, M., Stebler, M., Csúcs, G., Mayer, T. U., Zamboni, N., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.11.061 · Cited by 100 · see citing works
Regulation of rDNA transcription in response to growth factors, nutrients and energy
Kusnadi, E. P., Hannan, K. M., Hicks, R. J., Hannan, R. D., Pearson, R. B., & Kang, J. (2014) · Gene · doi:10.1016/j.gene.2014.11.010 · Cited by 95 · see citing works
Yerlikaya, S., Meusburger, M., Kumari, R., Huber, A., Anrather, D., Costanzo, M., Boone, C. M., Ammerer, G., Baranov, P. V., & Loewith, R. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-08-0594 · Cited by 89 · see citing works
RSK phosphorylates SOS1 creating 14-3-3-docking sites and negatively regulating MAPK activation
Saha, M., Carriere, A., Cheerathodi, M., Zhang, X., Lavoie, G., Rush, A. J., Roux, P. P., & Ballif, B. A. (2012) · Biochemical Journal · doi:10.1042/bj20120938 · Cited by 88 · see citing works
Self-citationGhalei, H., Schaub, F. X., Doherty, J. R., Noguchi, Y., Roush, W. R., Cleveland, J. L., Stroupe, M. E., & Karbstein, K. (2015) · The Journal of Cell Biology · doi:10.1083/jcb.201409056 · Cited by 86 · see citing works
Geerlings, T. H., Faber, A. W., Bister, M. D., Vos, J. C., & Raué, H. A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300759200 · Cited by 81 · see citing works
Chapter 2 Cell Signaling in Protein Synthesis
Mahoney, S. J., Dempsey, J. M., & Blenis, J. (2009) · Progress in molecular biology and translational science · doi:10.1016/s1877-1173(09)90002-3 · Cited by 78 · see citing works
Srivastava, L., Lapik, Y. R., Wang, M., & Pestov, D. G. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00226-10 · Cited by 73 · see citing works
Talkish, J., Zhang, J., Jakovljevic, J., Horsey, E., & Woolford, J. L. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks609 · Cited by 70 · see citing works
RSK regulates activated BRAF signalling to mTORC1 and promotes melanoma growth
Roméo, Y., Moreau, J., Zindy, P.-J., Saba-El-Leil, M. K., Lavoie, G., Dandachi, F., Baptissart, M., Borden, K. L. B., Meloche, S., & Roux, P. P. (2012) · Oncogene · doi:10.1038/onc.2012.312 · Cited by 64 · see citing works
Self-citationTwo orthogonal cleavages separate subunit RNAs in mouse ribosome biogenesis
Wang, M., Anikin, L., & Pestov, D. G. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku787 · Cited by 64 · see citing works
Sequential domain assembly of ribosomal protein S3 drives 40S subunit maturation
Mitterer, V., Murat, G., Réty, S., Blaud, M., Delbos, L., Stanborough, T., Bergler, H., Leulliot, N., Kressler, D., & Pertschy, B. (2016) · Nature Communications · doi:10.1038/ncomms10336 · Cited by 64 · see citing works
TOR regulates late steps of ribosome maturation in the nucleoplasm via Nog1 in response to nutrients
Honma, Y., Kitamura, A., Shioda, R., Maruyama, H., Ozaki, K., Oda, Y., Mini, T., Jenö, P., Maki, Y., Yonezawa, K., et al. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601262 · Cited by 62 · see citing works
Stefanovsky, V. Y., Langlois, F., Bazett‐Jones, D. P., Pelletier, G., & Moss, T. (2006) · Biochemistry · doi:10.1021/bi051782h · Cited by 56 · see citing works
Montellese, C., Montel-Lehry, N., Henras, A. K., Kutay, U., Gleizes, P., & O’Donohue, M.-F. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx253 · Cited by 56 · see citing works
Self-citationRegulation of RNA Polymerase III Transcription During Mammalian Cell Growth
Goodfellow, S. J., & White, R. J. (2007) · Cell Cycle · doi:10.4161/cc.6.19.4767 · Cited by 54 · see citing works
Human RioK3 is a novel component of cytoplasmic pre-40S pre-ribosomal particles
Belhabich-Baumas, K., Soudet, J., Caizergues‐Ferrer, M., Faubladier, M., Henry, Y. A. L., & Mougin, A. (2012) · RNA Biology · doi:10.4161/rna.18810 · Cited by 53 · see citing works
Self-citationMaturation of pre‐40S particles in yeast and humans
Cerezo, E. L., Plisson‐Chastang, C., Henras, A. K., Lebaron, S., Gleizes, P., O’Donohue, M.-F., Roméo, Y., & Henry, Y. A. L. (2018) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1516 · Cited by 52 · see citing works
Self-citationWyler, E., Zimmermann, M., Widmann, B., Gstaiger, M., Pfannstiel, J., Kutay, U., & Zemp, I. (2010) · RNA · doi:10.1261/rna.2325911 · Cited by 48 · see citing works
Asmal, M., Colgan, J. D., Naef, F., Yu, B., Lee, Y., Magnasco, M. O., & Luban, J. (2003) · Immunity · doi:10.1016/s1074-7613(03)00268-1 · Cited by 45 · see citing works
Stefanovsky, V. Y., & Moss, T. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn484 · Cited by 45 · see citing works
CK1δ and CK1ε are components of human 40S subunit precursors required for cytoplasmic 40S maturation
Zemp, I., Wandrey, F., Rao, S., Ashiono, C., Wyler, E., Montellese, C., & Kutay, U. (2014) · Journal of Cell Science · doi:10.1242/jcs.138719 · Cited by 44 · see citing works
A non-canonical mechanism for Crm1-export cargo complex assembly
Fischer, U., Schäuble, N., Schütz, S., Altvater, M., Chang, Y., Faza, M. B., & Panse, V. G. (2015) · eLife · doi:10.7554/elife.05745 · Cited by 44 · see citing works
Vanrobays, E., Leplus, A., Osheim, Y. N., Beyer, A. L., Wacheul, L., & Lafontaine, D. L. J. (2008) · RNA · doi:10.1261/rna.1176708 · Cited by 44 · see citing works
Mitterer, V., Shayan, R., Ferreira-Cerca, S., Murat, G., Enne, T., Rinaldi, D., Weigl, S., Omanic, H., Gleizes, P., Kressler, D., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10678-z · Cited by 44 · see citing works
Insights into the evolutionary conserved regulation of Rio ATPase activity
Knüppel, R., Christensen, R. H., Gray, F. C., Esser, D., Strauß, D., Medenbach, J., Siebers, B., MacNeill, S. A., LaRonde, N. A., & Ferreira-Cerca, S. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1236 · Cited by 42 · see citing works
Negative feedback via RSK modulates Erk‐dependent progression from naïve pluripotency
Nett, I. R. E., Mulas, C., Gatto, L., Lilley, K. S., & Smith, A. G. (2018) · EMBO Reports · doi:10.15252/embr.201745642 · Cited by 34 · see citing works
mTOR Signaling Regulates Nucleolar Targeting of the SUMO-Specific Isopeptidase SENP3
Raman, N., Nayak, A., & Müller, S. P. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.00801-14 · Cited by 33 · see citing works
Sriskanthadevan-Pirahas, S., Deshpande, R., Lee, B., & Grewal, S. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007202 · Cited by 31 · see citing works
Altered ERK/MAPK signaling in the hippocampus of the mrsk2_KO mouse model of Coffin‐Lowry syndrome
Schneider‐Anthony, A., Mehmood, T., Pannetier, S., & Hanauer, A. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07423.x · Cited by 30 · see citing works
Identification of distinct maturation steps involved in human 40S ribosomal subunit biosynthesis
Nieto, B., Gaspar, S. G., Moriggi, G., Pestov, D. G., Bustelo, X. R., & Dosil, M. (2020) · Nature Communications · doi:10.1038/s41467-019-13990-w · Cited by 30 · see citing works
Liu, T., Deng, M., Li, J., Tong, X., Qian, W., & Ye, X. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.250175 · Cited by 29 · see citing works
Zhang, Z., Liu, R., Townsend, P. A., & Proud, C. G. (2013) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2013.03.006 · Cited by 24 · see citing works
Interactions and activities of factors involved in the late stages of human 18S rRNA maturation
Sloan, K. E., Knox, A. A., Wells, G. R., Schneider, C., & Watkins, N. J. (2019) · RNA Biology · doi:10.1080/15476286.2018.1564467 · Cited by 22 · see citing works
Song, Y., Cheng, L., Jin, L., Xing, J., Sha, Z., Zhang, T., Ji, D., Yu, R., & Gao, S. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.15107 · Cited by 22 · see citing works
RIOK2: straddling the kinase/ATPase line
Asquith, C. R. M., East, M. P., & Zuercher, W. J. (2019) · Nature Reviews Drug Discovery · doi:10.1038/d41573-019-00107-7 · Cited by 17 · see citing works
In vitro dimerization of human RIO2 kinase
Maurice, F., Pérébaskine, N., Thore, S., & Fribourg, S. (2019) · RNA Biology · doi:10.1080/15476286.2019.1653679 · Cited by 7 · see citing works
Isfort, R. J., & Cody, D. B. (1992) · Cellular Signalling · doi:10.1016/0898-6568(92)90047-c · Cited by 5 · see citing works
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Bell, H. N., Rebernick, R. J., Goyert, J. W., Singhal, R., Kuljanin, M., Kerk, S. A., Huang, W., Das, N. K., Andren, A. C., Solanki, S. A., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.12.001 · Cited by 301 · see citing works
Mukhopadhyay, S., Huang, H.-Y., Lin, Z., Ranieri, M., Li, S., Sahu, S., Liu, Y., Ban, Y., Guidry, K., Hu, H., et al. (2023) · Cancer Research · doi:10.1158/0008-5472.can-23-2729 · Cited by 105 · see citing works
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Houlès, T., Lavoie, G., Nourreddine, S., Cheung, W., Vaillancourt-Jean, É., Guérin, C. M., Bouttier, M., Grondin, B., Lin, S., Saba-El-Leil, M. K., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-34179-8 · Cited by 40 · see citing works
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Levesque, S., Mayorga, D., Fiset, J.-P., Goupil, C., Duringer, A., Loiselle, A., Bouchard, E., Agudelo, D., & Doyon, Y. (2022) · Nature Communications · doi:10.1038/s41467-022-33669-z · Cited by 40 · see citing works
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Ghandadi, M., Dobi, A. L., & Malhotra, S. V. (2024) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2024.189100 · Cited by 14 · see citing works
Ma, H., Liu, C., Li, Z., Yu, Q., Xiong, H., Huang, C., Tan, L., Zhan, M., Zhang, Z., & Cai, Q. (2024) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2024.117166 · Cited by 11 · see citing works
Ma, M., Wang, F., Cui, P., Zhang, Y., Ma, H., He, Y., CHENG, Y. N., Huang, J., Wang, J., Wu, X., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-65012-7 · Cited by 8 · see citing works
Gao, Z., Xu, C., Fan, H., Wang, H., Wu, Z., Wu, S., & Bao, W. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232112712 · Cited by 8 · see citing works
Neuronal processes contain the essential components for the late steps of ribosome biogenesis
Fusco, C. M., Staab, A., Bourke, A. M., Tushev, G., Desch, K., Lins, É. M., Ciirdaeva, E., Dieck, S. T., Kaltenschnee, N., Heckel, A., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2502424122 · Cited by 7 · see citing works
MacMullan, M. A., Wang, P., & Graham, N. A. (2021) · Cytokine · doi:10.1016/j.cyto.2022.155958 · Cited by 7 · see citing works
Signaling to make human ribosomes: Connections between the cytoplasm and the nucleolus
Lawrence, I. R., Sutton, E. C., Bhaskar, S., & Baserga, S. J. (2026) · Molecular Cell · doi:10.1016/j.molcel.2026.01.007 · Cited by 6 · see citing works
Ribosome biogenesis and ribosomal proteins in cancer stem cells: a new therapeutic prospect
Samanta, P., Ghosh, R., Pakhira, S., Mondal, M., Biswas, S., Sarkar, R., Bhowmik, A., Saha, P., & Hajra, S. (2024) · Molecular Biology Reports · doi:10.1007/s11033-024-09963-y · Cited by 6 · see citing works
Identification of common genes and pathways between type 2 diabetes and COVID-19
Wang, Y., Li, K., Mo, S., Yao, P., Zeng, J., Lu, S., & Qin, S. (2024) · Frontiers in Genetics · doi:10.3389/fgene.2024.1249501 · Cited by 4 · see citing works
Ma, H., Huang, C., Gu, M., Wang, Y., Zhu, C., Zeng, H. D., Li, Z., Xiong, H., Wu, Y., Lai, Y., et al. (2025) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.5c01424 · Cited by 3 · see citing works
Drastichová, Z., Trubacova, R., & Novotný, J. (2022) · Cells · doi:10.3390/cells11091473 · Cited by 3 · see citing works
Zhao, R., Lu, Y., Xu, Q., Ren, H., Li, H., Gao, J., Cui, H., Yuan, Z., Cao, B., & Wei, B. (2025) · International Journal of Surgery · doi:10.1097/js9.0000000000004080 · Cited by 2 · see citing works
Xie, P., Pei, Y., Xu, L. N., Shan, Y., & Cao, X. (2026) · Metabolites · doi:10.3390/metabo16070438 · Cited by 2 · see citing works
Thermo-sensing mechanisms of splicing control by nuclear stress bodies
Ueno, T., Adachi, S., Taniguchi, I., Noda, N. N., Ninomiya, K., & Hirose, T. (2026) · Molecular Cell · doi:10.1016/j.molcel.2026.06.034 · Cited by 1 · see citing works
Fluoxetine promotes lysosome biogenesis via regulation of a RIOK2-TFEB axis
Lin, L., Zhou, L., Cang, R., Han, B., & Li, Y. (2025) · Medicine in Drug Discovery · doi:10.1016/j.medidd.2025.100239
Ma, X., Wen, Z., Wang, Z., Peng, Z., Wu, D., Wang, J., & Liu, B. (2026) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2026.03.047
Phosphorylation Patterns of Preribosomal Proteins Associated with the RNA Exosome
Almeida, F. A., Neto, V. G., Jantsch, R. B., Barros, M. R. A., Cepeda, L. P. P., Queiroz, B. R. S., Machado, A. B. E., Menezes, A. P. D. J., da Cunha, J. P., & Oliveira, C. C. (2026) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6c00095
von Blottnitz, K. I. B., Honemann‐Capito, M., Hackert, P., Dybkov, O., Lenz, C., Bohnsack, M. T., Lorenz, S. E., Urlaub, H., Schneider, C., & Bohnsack, K. E. (2026) · RNA · doi:10.1261/rna.081089.126
Ganbold, M., Sasaki, K., 大川, 和., Kobayashi, M., & Isoda, H. (2026) · Nutrients · doi:10.3390/nu18193285
Khan, N. A., Fahma, A., Gopalakrishnan, A. P., Sambreena, A., Raju, R., & Rajeev, A. C. (2026) · BioTech · doi:10.3390/biotech15040095
- Authors
- Cerezo, E. L., Houles, T., Lié, O., Sarthou, M.-K., Audoynaud, C., Lavoie, G., Halladjian, M., Cantaloube, S., Froment, C., Burlet-Schiltz, O., Henry, Y., Roux, P. P., Henras, A. K., & Romeo, Y.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Institute for Research in Immunology and Cancer (CA)
- Corresponding author
- Henras, Anthony K.
- ORCID
- Venue
- PLOS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2021-06-14
- Volume
- 17
- Issue
- 6
- Pages
- e1009583
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC8224940
- OpenAlex
- W3167931457
- Cited by
- 26
- References
- 85
- Citations by year
- 2026: 9 · 2025: 5 · 2024: 4 · 2023: 1 · 2022: 5 · 2021: 2
- FWCI
- 0.94
- Type
- journal article
- Language
- en
- Update notices
- new_version (2021-06-24)
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- ANR (ANR-10-INBS-08)
- Ligue Contre le Cancer
- Région Midi-Pyrénées
- FEDER
- Toulouse Métropole
- Canadian Institutes for Health Research (MOP-142374 and PJT-152995)
- Natural Sciences and Engineering Research Council of Canada
- Fonds de Recherche du Québec - Santé
- Ministère de l’Enseignement Supérieur et de la Recherche
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- RSK, ribosome biogenesis, small ribosomal subunit, post-transcriptional regulation, RAS/MAPK pathway, protein phosphorylation, cell proliferation, protein synthesis
- MeSH terms
- Humans, Mutation, Phosphorylation, Substrate Specificity, Transcription, Genetic, Signal Transduction, Protein Serine-Threonine Kinases, Mitogen-Activated Protein Kinases, Protein Transport, Ribosome Subunits, Small, HEK293 Cells
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