The DOI matches its Crossref record; 62 of the 62 references it cites were found in a registry or an index.
Ribonomic Analysis of Human Pum1 Reveals cis-trans Conservation across Species despite Evolution of Diverse mRNA Target Sets
Open accessAbstract
PUF family proteins are among the best-characterized regulatory RNA-binding proteins in nonmammalian species, but relatively little is known about mRNA targets or functions of mammalian PUF proteins. In this study, we used ribonomic analysis to identify and analyze mRNAs associated with ribonucleoproteins containing an endogenous human PUF protein, Pum1. Pum1-associated mRNAs were highly enriched for genes encoding proteins that function in transcriptional regulation and cell cycle/proliferation, results consistent with the posttranscriptional RNA regulon model and the proposed ancestral functions of PUF proteins in stem cell biology. Analysis of 3' untranslated region sequences of Pum1-associated mRNAs revealed a core Pum1 consensus sequence, UGUAHAUA. Pum1 knockdown demonstrated that Pum1 enhances decay of associated mRNAs, and relocalization of Pum1 to stress granules suggested that Pum1 functions in repression of translation. This study is the first in vivo genome-wide mRNA target identification of a mammalian PUF protein and provides direct evidence that human PUF proteins regulate stability of associated mRNAs. Comparison of Pum1-associated mRNAs to mRNA targets of PUF proteins from Saccharomyces cerevisiae and Drosophila melanogaster demonstrates how a well-conserved RNA-binding domain and cognate binding sequence have been evolutionarily rewired to regulate the collective expression of different sets of functionally related genes.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
In the citing paper
“motifs for the alternative splicing factorsRBFOX1, RBFOX2 and RBFOX3 (ref. 4) are conserved in introns downstream of alternative exons, whereas sites for the stability/translation factors PUM1 and PUM2 are most highly conserved in 3′ UTRs24,25”
From A compendium of RNA-binding motifs for decoding gene regulation (2013) · cites this paper as [25]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625
Mootha, V. K., Lindgren, C. M., Eriksson, K.-F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstråle, M., Laurila, E., et al. (2003) · Nature Genetics · doi:10.1038/ng1180 · Cited by 10,197
MEME: discovering and analyzing DNA and protein sequence motifs
Bailey, T. L., Williams, N., Misleh, C., & Li, W. W. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl198 · Cited by 2,671
WebGestalt: an integrated system for exploring gene sets in various biological contexts
Zhang, B., Kirov, S. A., & Snoddy, J. R. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki475 · Cited by 1,803
III. Contributions to the mathematical theory of evolution
Pearson, K. (1894) · Philosophical Transactions of the Royal Society of London (A ) · doi:10.1098/rsta.1894.0003 · Cited by 1,571
RNA regulons: coordination of post-transcriptional events
Keene, J. D. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2111 · Cited by 1,321
Self-citationAnderson, P., & Kedersha, N. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200512082 · Cited by 984
Lin, H., & Spradling, A. C. (1997) · Development · doi:10.1242/dev.124.12.2463 · Cited by 694
Mammalian Stress Granules and Processing Bodies
Kedersha, N., & Anderson, P. (2007) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(07)31005-7 · Cited by 672
Gerber, A. P., Herschlag, D., & Brown, P. O. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020079 · Cited by 670
Flagged first, then by citations
Research works printed but not linked: 4
- DeGregori J., 2006, Curr. Mol. Med., 6, 739
- Spik A., 2006, Reprod. Biol., 6, 103
- White E. K., 2001, RNA, 7, 1855
- Zamore P. D., 1997, RNA, 3, 1421
Cited by
Sorted by citations
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
Noncoding RNA NORAD Regulates Genomic Stability by Sequestering PUMILIO Proteins
Lee, S., Kopp, F. B., Chang, T.-C., Sataluri, A., Chen, B., Sivakumar, S., Yu, H., Xie, Y., & Mendell, J. T. (2015) · Cell · doi:10.1016/j.cell.2015.12.017 · Cited by 892
MicroRNA regulation by RNA-binding proteins and its implications for cancer
van Kouwenhove, M., Kedde, M., & Agami, R. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3107 · Cited by 617
“In fact, several other cell cycle regulators have been identified as human PUM1 targets and are repressed through their mRNA 3′ UT”
BackgroundA Pumilio-induced RNA structure switch in p27-3′ UTR controls miR-221 and miR-222 accessibility
Kedde, M., van Kouwenhove, M., Zwart, W. T., Vrielink, J. A. F. O., Elkon, R., & Agami, R. (2010) · Nature Cell Biology · doi:10.1038/ncb2105 · Cited by 406
“Pumilio-1 (PUM1) is a ubiquitously expressed RBP that was shown to interact with p27-3′ UT”
BackgroundPARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data
Corcoran, D. L., Georgiev, S., Mukherjee, N., Gottwein, E., Skalsky, R. L., Keene, J. D., & Ohler, U. (2011) · Genome biology · doi:10.1186/gb-2011-12-8-r79 · Cited by 342
“The functions of Pumilio are widely studied in a variety of species, and its global RNA targeting properties has been examined across a large phylogeny [12-17].”
BackgroundSelf-citationPUF proteins: repression, activation and mRNA localization
Quenault, T., Lithgow, T. J., & Traven, A. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.09.013 · Cited by 275
Galgano, A., Forrer, M., Jaśkiewicz, Ł., Kanitz, A., Zavolan, M., & Gerber, A. P. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003164 · Cited by 279
“We have systematically analyzed the mRNAs associated with the two human Pumilio RNA-binding proteins, PUM1 and PUM2 in HeLa S3 cancer cells, using a method that combines the recovery of endogenous RNP complexes and DNA microarray analysis of the associated mRNAs [2,44,60,61,62].”
MethodResultInfluentialAntiviral innate immunity and stress granule responses
Onomoto, K., Yoneyama, M., Fung, G., Kato, H., & Fujita, T. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.07.006 · Cited by 246
Human Pumilio Proteins Recruit Multiple Deadenylases to Efficiently Repress Messenger RNAs
Van Etten, J., Schagat, T. L., Hrit, J., Weidmann, C. A., Brumbaugh, J., Coon, J. J., & Goldstrohm, A. C. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.373522 · Cited by 205
Post-transcriptional Regulatory Functions of Mammalian Pumilio Proteins
Goldstrohm, A. C., Hall, T. M. T., & McKenney, K. M. (2018) · Trends in Genetics · doi:10.1016/j.tig.2018.09.006 · Cited by 198
Griesemer, D. S., Xue, J. R., Reilly, S. K., Ulirsch, J. C., Kukreja, K., Davis, J. R., Kanai, M., Yang, D. K., Butts, J. C., Guney, M. H., et al. (2021) · Cell · doi:10.1016/j.cell.2021.08.025 · Cited by 176
Predicting in vivo binding sites of RNA-binding proteins using mRNA secondary structure
Li, X., Quon, G., Lipshitz, H. D., & Morris, Q. (2010) · RNA · doi:10.1261/rna.2017210 · Cited by 181
Roles of Puf proteins in mRNA degradation and translation
Miller, M. A., & Olivas, W. M. (2010) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.69 · Cited by 159
Stress-Dependent Coordination of Transcriptome and Translatome in Yeast
Halbeisen, R. E., & Gerber, A. P. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000105 · Cited by 141
“Intriguingly, we and others have shown that regulatory RBPs often bind to messages that encode functionally related proteins [2,11–14,64,65].”
BackgroundLee, J. E., Lee, J. Y., Wilusz, J., Tian, B., & Wilusz, C. J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011201 · Cited by 133
“A subset of CUGBP1 targets are shared with HuR and/or Pum1 The sequence preferences of CUGBP1 overlap with those of HuR and Pum1 proteins, both of which are also able to bind to elements with a core UGU trinucleotide.”
BackgroundResultInfluentialMassively parallel functional annotation of 3′ untranslated regions
Zhao, W., Pollack, J. L., Blagev, D. P., Zaitlen, N., McManus, M. T., & Erle, D. J. (2014) · Nature Biotechnology · doi:10.1038/nbt.2851 · Cited by 125
“We used the UGUANAUA motif identified in human Pumilio immunoprecipitation experiments 9, 19, 20 to predict elements recognized by Pumilio.”
Pumilio 1 Suppresses Multiple Activators of p53 to Safeguard Spermatogenesis
Chen, D., Zheng, W., Lin, A., Uyhazi, K. E., Zhao, H., & Lin, H. (2012) · Current Biology · doi:10.1016/j.cub.2012.01.039 · Cited by 126
“This motif predominantly resides in their 3′UTRs (Figure 2C), and is the same as those found in mRNA targets of yeast Puf3 [20], Drosophila Pum [9], and human PUM1 and PUM2 [18, 19], indicating that the Pum binding motif is highly conserved.”
Advancing the functional utility of PAR-CLIP by quantifying background binding to mRNAs and lncRNAs
Friedersdorf, M. B., & Keene, J. D. (2014) · Genome biology · doi:10.1186/gb-2014-15-1-r2 · Cited by 119
“…settings to define binding sites (Additional files 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16,17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62, 63, 64, 65 and 66).”
Self-citationAnalysis of CUGBP1 Targets Identifies GU-Repeat Sequences That Mediate Rapid mRNA Decay
Rattenbacher, B., Beisang, D. J., Wiesner, D. L., Jeschke, J. C., von Hohenberg, M., Louis, I. V.-S., & Bohjanen, P. R. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00624-10 · Cited by 123
Harnessing CRISPR/Cas systems for programmable transcriptional and post-transcriptional regulation
Mahas, A., Neal Stewart, C., & Mahfouz, M. M. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2017.11.008 · Cited by 110
“For example, PUF proteins can only recognize eight adjacent bases, which leads them to recognize a wide range of transcripts (Galgano et al., 2008; Morris et al., 2008).”
BackgroundCooperativity in RNA-Protein Interactions: Global Analysis of RNA Binding Specificity
Campbell, Z. T., Bhimsaria, D., Valley, C. T., Rodríguez‐Martínez, J. A., Menichelli, E., Williamson, J. R., Ansari, A. Z., & Wickens, M. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.04.003 · Cited by 119
“Second, many mRNAs that bind a regulatory protein in vivo, as judged by coimmunopurification studies, lack a consensus binding site (Galgano et al., 2008; Gerber et al., 2004, 2006; Hafner et al., 2010; Kershner and Kimble, 2010; Morris et al., 2008).”
BackgroundInfluentialGenome-wide analysis of mRNA targets for Caenorhabditis elegans FBF, a conserved stem cell regulator
Kershner, A. M., & Kimble, J. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000495107 · Cited by 115
“This enrichment suggests a role for FBF targets in regulation of other genes or complexes and that FBF is a “regulator of regulators,” as previously proposed for human PUM1 (17).”
BackgroundResultInfluentialStructural basis for specific recognition of multiple mRNA targets by a PUF regulatory protein
Wang, Y., Opperman, L., Wickens, M., & Hall, T. M. T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812076106 · Cited by 113
“elegans to PUMILIO, recognizes a core 8-nt sequence (20), 5 -UGUANAUA-3 (4, 30–32), the same as that seen by PUM1 (30).”
BackgroundSystematic analysis of posttranscriptional gene expression
Morris, A. R., Mukherjee, N., & Keene, J. D. (2009) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.54 · Cited by 112
“HeLa — Pum1 Cell cycle and transcription factors UGUAHAUA E, M (56)”
BackgroundSelf-citationLive‐cell imaging of viral RNA genomes using a Pumilio‐based reporter
Tilsner, J., Linnik, O., Christensen, N. M., Bell, K., Roberts, I. M., Lacomme, C., & OPARKA, K. J. (2008) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03720.x · Cited by 110
Trans-acting proteins regulating mRNA maturation, stability and translation in trypanosomatids
Krämer, S., & Carrington, M. (2010) · Trends in Parasitology · doi:10.1016/j.pt.2010.06.011 · Cited by 109
Identification of diverse target RNAs that are functionally regulated by human Pumilio proteins
Bohn, J. A., Etten, J. L. V., Schagat, T. L., Bowman, B. M., McEachin, R. C., Freddolino, L., & Goldstrohm, A. C. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1120 · Cited by 104
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
“…regulators of gene expression, a phenomena generally described as “regulators of regulators” (Tenenbaum et al., 2000; Lopez de Silanes et al., 2004; Mesarovic et al., 2004; Penalva et al., 2004; Gerber et al., 2006; Keene, 2007a; Pullman et al., 2007; Morris et al., 2008; Galgano et al., 2008).”
BackgroundSelf-citationPUMILIO hyperactivity drives premature aging of Norad-deficient mice
Kopp, F. B., YALVAÇ, M. E., Chen, B., Zhang, H., 이성율, Gillett, F. A., Elguindy, M. M., Sivakumar, S., Yu, H., Xie, Y., et al. (2019) · eLife · doi:10.7554/elife.42650 · Cited by 94
Post-transcriptional RNA regulons affecting cell cycle and proliferation
Blackinton, J. G., & Keene, J. D. (2014) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2014.05.014 · Cited by 95
“A good example of RNAprotein rewiring have been observed with PUF3 family RBPs, with changes in classes of regulatory targets within fungal species [31,32] as well as across many other metazoan species [30,33].”
BackgroundSelf-citationPost‐transcriptional regulation of the Ras‐ERK/MAPK signaling pathway
Whelan, J. T., Hollis, S., Seok, D., Asch, A. S., & Lee, M. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.22899 · Cited by 94
“1B, E), but it is unknown if LARP-1 directly binds to mpk-1 and let-60 mRNAs (Nykamp et al., 2008).”
BackgroundInfluentialMiao, J., Li, J., Fan, Q., Li, X., Li, X., & Cui, L. (2010) · Journal of Cell Science · doi:10.1242/jcs.059824 · Cited by 94
Tam, P., Barrette‐Ng, I. H., Simon, D. M., Tam, M. W., Ang, A. L., & Muench, D. G. (2010) · BMC Plant Biology · doi:10.1186/1471-2229-10-44 · Cited by 99
“instance, human Pum1 binds hundreds of mRNA targets in vivo [17,18], as do Puf proteins from Drosophila, C.”
BackgroundMinireview: Global Regulation and Dynamics of Ribonucleic Acid
Keene, J. D. (2010) · Endocrinology · doi:10.1210/en.2009-1250 · Cited by 92
“Recent studies with activated T cells have examined the dynamics of global mRNA populations using a probabilistic approach applying Gaussian mixture modeling and related statistical methods (27, 47).”
MethodSelf-citationWho Regulates Whom? An Overview of RNA Granules and Viral Infections
Poblete, N., Prades, Y., Vera‐Otarola, J., Soto‐Rifo, R., & Valiente‐Echeverría, F. (2016) · Viruses · doi:10.3390/v8070180 · Cited by 89
A GC-rich sequence feature in the 3′ UTR directs UPF1-dependent mRNA decay in mammalian cellsPreprint
Imamachi, N., Salam, K. A., Suzuki, Y., & Akimitsu, N. (2016) · Genome Research · doi:10.1101/gr.206060.116 · Cited by 85
“In contrast, mRNAs with a binding motif for PUM1, a well-known mRNA decay factor (Morris et al. 2008), were not significantly stabilized after the depletion of UPF1 and bound to neither UPF1 nor p-UPF1 (Fig.”
BackgroundCoordinated posttranscriptional mRNA population dynamics during T‐cell activation
Mukherjee, N., Lager, P. J., Friedersdorf, M. B., Thompson, M. A., & Keene, J. D. (2009) · Molecular Systems Biology · doi:10.1038/msb.2009.44 · Cited by 87
“…the probability of HuR association and mRNA abundance (Figure 2C, red numbers), indicating that RIP chip successfully isolated specific subsets of mRNAs that were not quantitatively representative of total mRNA, consistent with our earlier studies (Tenenbaum et al, 2000; Morris et al, 2008).”
BackgroundMethodResultInfluentialSelf-citationWeidmann, C. A., Raynard, N. A., Blewett, N. H., Etten, J. V., & Goldstrohm, A. C. (2014) · RNA · doi:10.1261/rna.046029.114 · Cited by 83
“These observations held true for target mRNAs with a minimal 3′ UTR with PRE elements and for a target mRNA that contains the 3′ UTR of the natural Pum target mRNA, Hunchback.”
InfluentialAlternate Modes of Cognate RNA Recognition by Human PUMILIO Proteins
Lu, G., & Hall, T. M. T. (2011) · Structure · doi:10.1016/j.str.2010.12.019 · Cited by 84
“This preference is consistent with the low frequency of appearance of C at position 8 in mRNAs associated with PUM1 (Morris et al., 2008).”
BackgroundInfluentialLaver, J. D., Li, X., Ancevicius, K., Westwood, J. T., Smibert, C. A., Morris, Q., & Lipshitz, H. D. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt702 · Cited by 86
Webster, M. W., Stowell, J. A. W., & Passmore, L. A. (2019) · eLife · doi:10.7554/elife.40670 · Cited by 80
Puf Mediates Translation Repression of Transmission-Blocking Vaccine Candidates in Malaria Parasites
Miao, J., Fan, Q., Parker, D. M., Li, X., Li, J., & Cui, L. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003268 · Cited by 75
Post-transcriptional Control of Gene Expression During Mouse Oogenesis
Clarke, H. J. (2012) · Results and problems in cell differentiation · doi:10.1007/978-3-642-30406-4_1 · Cited by 78
Understanding and engineering RNA sequence specificity of PUF proteins
Lu, G., Dolgner, S. J., & Hall, T. M. T. (2009) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2008.12.009 · Cited by 76
A Quantitative and Predictive Model for RNA Binding by Human Pumilio Proteins
Jarmoskaite, I., Denny, S. K., Vaidyanathan, P. P., Becker, W. R., Andreasson, J. O. L., Layton, C. J., Kappel, K., Shivashankar, V., Sreenivasan, R., Das, R., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.04.012 · Cited by 76
Pseudouridine and N 6 -methyladenosine modifications weaken PUF protein/RNA interactions
Vaidyanathan, P. P., AlSadhan, I., Merriman, D. K., Al‐Hashimi, H. M., & Herschlag, D. (2017) · RNA · doi:10.1261/rna.060053.116 · Cited by 73
“Human Pumilio proteins, like other PUF family RBPs, recognize a highly conserved core motif, typified by the sequence UGUA(N)nAUA (Wickens et al. 2002; Gerber et al. 2004; Galgano et al. 2008; Morris et al. 2008).”
BackgroundThe Interplay between the RNA Decay and Translation Machinery in EukaryotesPreprint
Heck, A. M., & Wilusz, J. (2018) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a032839 · Cited by 77
“1997) and modulates mRNA fate through 30 UTR interactions (Morris et al. 2008; Hafner et al. 2010).”
BackgroundHuman Pumilio proteins directly bind the CCR4-NOT deadenylase complex to regulate the transcriptome
Enwerem-Lackland, I., Elrod, N. D., Chang, C.-T., Lin, A., Ji, P., Bohn, J. A., Levdansky, Y., Wagner, E. J., Valkov, E., & Goldstrohm, A. C. (2021) · RNA · doi:10.1261/rna.078436.120 · Cited by 63
“…repression, we compared the upregulated gene set (Figure S2E: “PUM1&2 RNAi”) with previously identified genes that contain PREs (Figure S2E: “PRE”) and that are bound by PUMs (Figure S2E: “Bound”)(Galgano et al. 2008; Morris, Mukherjee, and Keene 2008; Hafner et al. 2010; Bohn et al. 2018).”
InfluentialAddressing mRNAs to the ER: cis sequences act up!
Kraut‐Cohen, J., & Gerst, J. E. (2010) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2010.02.006 · Cited by 69
Heikkilä, O., Susi, P., Tevaluoto, T., Härmä, H., Marjomäki, V., Hyypiä, T., & Kiljunen, S. (2010) · Journal of Virology · doi:10.1128/jvi.01340-09 · Cited by 67
“However, as PUM1 was recently shown to be a central regulator that regulates the expression of over 10% of human genes (43), it is very difficult to deduce the reason for this suppression.”
BackgroundGlobal coordination of transcriptional control and mRNA decay during cellular differentiation
Amorim, M. J., Cotobal, C., Duncan, C. D. S., & Mata, J. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.38 · Cited by 67
“…2008 for reviews and Hogan et al, 2008 for a recent example), including a few regulators of RNA decay (the Puf1, HuR, tristetraprolin and AUF1 proteins; Lopez de Silanes et al, 2004; Galgano et al, 2008; Mazan-Mamczarz et al, 2009; Morris et al, 2008; Stoecklin et al, 2008; Mukherjee et al, 2009).”
BackgroundAn Important Role of Pumilio 1 in Regulating the Development of the Mammalian Female Germline1
Mak, W., Fang, C., Holden, T. M., Dratver, M. B., & Lin, H. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.115.137497 · Cited by 64
“Therefore, there may be redundancy in the function of the PUM proteins, such that some of the function of PUM may be partially compensated by PUM2 in its absence, but lack of PUM2 can be fully compensated by the presence of PUM1 [23, 39, 40].”
BackgroundPUMILIO proteins promote colorectal cancer growth via suppressing p21
Gong, Y., Liu, Z., Yuan, Y., Yang, Z., Zhang, J., Lu, Q., Wang, W., Fang, C., Lin, H., & Liu, S. (2022) · Nature Communications · doi:10.1038/s41467-022-29309-1 · Cited by 65
“Before that, Input Ct value was corrected following the equation: Ctcorrected= Ctinput − log2 (20).”
MethodNew insights into the cellular temporal response to proteostatic stress
Rendleman, J., Cheng, Z., Maity, S., Kastelić, N., Munschauer, M., Allgoewer, K., Teo, G., Zhang, Y. B. M., Lei, A., Parker, B. J., et al. (2018) · eLife · doi:10.7554/elife.39054 · Cited by 58
Pum2 Shapes the Transcriptome in Developing Axons through Retention of Target mRNAs in the Cell Body
Martínez, J. C., Randolph, L. K., Iascone, D. M., Pernice, H. F., Polleux, F., & Hengst, U. (2019) · Neuron · doi:10.1016/j.neuron.2019.08.035 · Cited by 57
“(D) FIRE was run in non-discovery mode on a genome-wide subcellular localizat tested: UGUA[ACU]AU[AU] (Pum2 preferred; top row) and UGUA[ACU]AUA (Pum (E) FIRE was run in non-discovery mode on a primary cortical neuron genome-w were tested: UGUA[ACU]AU[AU] (Pum2 preferred; top row) and UGUA[ACU]AUA closely resembles th…”
BackgroundMethodPerspectives on the ARE as it turns 25 years old
Beisang, D. J., & Bohjanen, P. R. (2012) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1125 · Cited by 56
Evolutionary Conservation and Diversification of Puf RNA Binding Proteins and Their mRNA Targets
Hogan, G. J., Brown, P. O., & Herschlag, D. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002307 · Cited by 54
“Fewer than 20% of the targets of the Puf3 orthologs in humans and flies are themselves orthologs [24,29], and the functional themes of their mRNA targets in flies and humans starkly contrast with those for yeast Puf3 [24,27,29].”
BackgroundResultInfluentialStacking interactions in PUF–RNA complexes
Koh, Y. Y., Wang, Y., Qiu, C., Opperman, L., Gross, L., Hall, T. M. T., & Wickens, M. (2011) · RNA · doi:10.1261/rna.2540311 · Cited by 54
DRIMust: a web server for discovering rank imbalanced motifs using suffix trees
Leibovich, L., Paz, I., Yakhini, Z., & Mandel‐Gutfreund, Y. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt407 · Cited by 54
“Similarly, messenger RNA targets of RBPs are studied using techniques like RNA immunoprecipitation (RIP)-chip (8), crosslinking and immunoprecipitation (CLIP) (9) and photo activatable-ribonucleoside-enhanced crosslinking and immunoprecipitation (PAR-CLIP) (10).”
MethodThe PUF binding landscape in metazoan germ cells
Prasad, A. K., Porter, D. F., Kroll-Conner, P., Mohanty, I., Ryan, A. R., Crittenden, S. L., Wickens, M., & Kimble, J. E. (2016) · RNA · doi:10.1261/rna.055871.116 · Cited by 50
“…cells all suggested that PUF proteins are broad-spectrum regulators of the genome, associating with RNAs from 7% to 11% of an organism’s genes (Gerber et al. 2004, 2006; Galgano et al. 2008; Morris et al. 2008; Hafner et al. 2010; Kershner and Kimble 2010; Chen et al. 2012; Wilinski et al. 2015).”
BackgroundLin, K., Qiang, W., Zhu, M., Ding, Y., Shi, Q., Chen, X., Zsíros, E., Wang, K., Yang, X., Kurita, T., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.111 · Cited by 52
“Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP.”
BackgroundInfluentialUyhazi, K. E., Yang, Y., Liu, N., Qi, H., Huang, X., Mak, W., Weatherbee, S. D., de Prisco, N., Gennarino, V. A., Song, X., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1916471117 · Cited by 54
Hu, Y., Tan, L., Chen, X., Liu, Z., Min, S., Zeng, Q., Shen, H., & Deng, H. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-01531 · Cited by 49
Quantifying RNA binding sites transcriptome-wide using DO-RIP-seq
Nicholson, C. O., Friedersdorf, M. B., & Keene, J. D. (2016) · RNA · doi:10.1261/rna.058115.116 · Cited by 49
“…be defined as RNA targets based on whether they contain a single mRNA binding site, it is more robust to define RNA targets by quantifying binding of the whole transcript by the ratio of RBP binding relative to a negative control (Tenenbaum et al. 2000; Morris et al. 2008; Mukherjee et al. 2009).”
InfluentialSelf-citationGermline Stem Cells and Their Regulation in the Nematode Caenorhabditis elegans
Kershner, A. M., Crittenden, S. L., Friend, K., Sorensen, E. B., Porter, D. F., & Kimble, J. E. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-6621-1_3 · Cited by 45
Valley, C. T., Porter, D. F., Qiu, C., Campbell, Z. T., Hall, T. M. T., & Wickens, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200521109 · Cited by 45
Lu, Z., Guan, X., Schmidt, C. A., & Matera, A. G. (2014) · Genome biology · doi:10.1186/gb-2014-15-1-r7 · Cited by 46
“For example, several studies on the RNA targets of Puf family proteins in yeast, fruit fly and human suggest that even though the binding sites of the proteins are conserved, the target mRNAs are not [41,80,81].”
BackgroundMethodPUM1 promotes ovarian cancer proliferation, migration and invasion
Guan, X., Chen, S., Liu, Y., Wang, L., Zhao, Y., & Zong, Z. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.02.078 · Cited by 45
A single C. elegans PUF protein binds RNA in multiple modes
Koh, Y. Y., Opperman, L., Stumpf, C. R., Mandan, A., Keleş, S., & Wickens, M. (2009) · RNA · doi:10.1261/rna.1545309 · Cited by 45
“2004) to more than 1000 in humans (Galgano et al. 2008; Morris et al. 2008).”
BackgroundAntagonistic and cooperative AGO2-PUM interactions in regulating mRNAs
Sternburg, E. L., Estep, J. A., Nguyen, D. K., Li, Y., & Karginov, F. V. (2018) · Scientific Reports · doi:10.1038/s41598-018-33596-4 · Cited by 42
Adrian‐Kalchhauser, I., Farley, B. M., Pauli, S., Ryder, S. P., & Ciosk, R. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.263 · Cited by 41
“The regulation of Cip/Kip mRNAs by PUF proteins appears to be evolutionarily conserved (Morris et al, 2008).”
BackgroundGinter-Matuszewska, B., Kusz-Zamelczyk, K., Spik, A., Grzeszkowiak, D., Rembiszewska, A., Kupryjańczyk, J., & Jaruzelska, J. (2011) · Histochemistry and Cell Biology · doi:10.1007/s00418-011-0842-y · Cited by 42
“gets of human PUMILIO1 and PUMILIO2 proteins were identiWed in HeLa cells (Morris et al. 2008; Galgano et al. 2008).”
BackgroundHafezqorani, S., Lafzi, A., de Bruin, R. G., van Zonneveld, A. J., van der Veer, E. P., Son, Y. A., & Kazan, H. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw048 · Cited by 41
Noncoding RNAs in Cancer Development
Lin, C., & He, L. (2016) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-050216-034443 · Cited by 42
“PUM proteins are RNA-binding proteins that associate with specific mRNAs at their 3′ untranslated regions (UTRs) through Pumilio response elements to promote mRNA degradation (Morris et al. 2008).”
BackgroundArchitecture and dynamics of overlapped RNA regulatory networks
Lapointe, C. P., Preston, M. A., Wilinski, D., Saunders, H. A. J., Campbell, Z. T., & Wickens, M. (2017) · RNA · doi:10.1261/rna.062687.117 · Cited by 39
“Individual PUF proteins bind hundreds of mRNAs, most commonly through specific sequences present in their 3ʹ untranslated regions (UTRs) (Gerber et al. 2004; Gerber et al. 2006; Galgano et al. 2008; Hogan et al. 2008; Morris et al. 2008; Hafner et al. 2010; Kershner and Kimble 2010; Chen et al. 2012; Lapointe et al. 2…”
BackgroundZhang, Y., He, X., Qin, S., Mo, H., Li, X., Wu, F., Zhang, J., Li, X., Mao, L., Peng, Y.-Q., et al. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2019.11.025 · Cited by 40
Devaux, F., Lelandais, G., Garcia, M., Goussard, S., & Jacq, C. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.09.030 · Cited by 44
Shigunov, P., Sotelo-Silveira, J. R., Kuligovski, C., de Aguiar, A. M., Rebelatto, C. L. K., Moutinho, J. A., Brofman, P. R. S., Krieger, M. A., Goldenberg, S., Munroe, D. J., et al. (2011) · Stem Cells and Development · doi:10.1089/scd.2011.0143 · Cited by 38
“PUF proteins have been described as regulators of regulators [30].”
PUF-8 suppresses the somatic transcription factor PAL-1 expression in C. elegans germline stem cells
Rana, M., Agarwal, P., & Subramaniam, K. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.09.021 · Cited by 36
“A few large-scale biochemical approaches have identified a number of mRNAs, representing most known cellular processes, as potential PUF targets (Galgano et al., 2008; Gerber et al., 2004, 2006; Kershner and Kimble, 2010; Morris et al., 2008).”
Havel, V. E., Wool, N. K., Ayad, D., Downey, K. M., Wilson, C. F., Larsen, P. E., Djordjevic, J. T., & Panepinto, J. C. (2011) · Eukaryotic Cell · doi:10.1128/ec.00006-11 · Cited by 33
Tinkering Evolution of Post-Transcriptional RNA Regulons: Puf3p in Fungi as an Example
Jiang, H., Guan, W., & Gu, Z. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001030 · Cited by 31
“In humans, two paralogous PUF proteins (Pum1p and Pum2p), which interact with the microRNA system in post-transcriptional regulation, share the same binding-element with yeast Puf3p and bind to mRNAs from genes that function in transcriptional regulation and cell proliferation [19,23].”
BackgroundFunctional and molecular characterization of the conserved Arabidopsis PUMILIO protein, APUM9
Nyikó, T., Auber, A., & Bucher, E. (2019) · Plant Molecular Biology · doi:10.1007/s11103-019-00853-7 · Cited by 30
“Putative PREs can be detected in a large fraction of genes (approximately 7–11%) in all studied model organisms (Galgano et al. 2008; Gerber et al. 2006; Kershner and Kimble 2010; Morris et al. 2008; Wilinski et al. 2015).”
BackgroundDivergent RNA binding specificity of yeast Puf2p
Yosefzon, Y., Koh, Y. Y., Chritton, J. J., Atir-Lande, A., Leibovich, L., Bar‐Ziv, L., Petzold, C., Yakhini, Z., Mandel‐Gutfreund, Y., Wickens, M., et al. (2011) · RNA · doi:10.1261/rna.2700311 · Cited by 30
“The binding sites of several PUF proteins have been identified biochemically and through in-formatics (Gerber et al. 2004; Bernstein et al. 2005; Opperman et al. 2005; Galgano et al. 2008; Hogan et al. 2008; Morris et al. 2008; Stumpf et al. 2008a; Koh et al. 2009).”
BackgroundRole of PUM RNA-Binding Proteins in Cancer
Smialek, M. J., Ilaslan, E., Sajek, M. P., & Jaruzelska, J. (2021) · Cancers · doi:10.3390/cancers13010129 · Cited by 29
“Deadenylation is followed mostly by degradation [18,19], which is in line with the finding Figure 1.”
BackgroundResultWolfe, M. B., Schagat, T. L., Paulsen, M. T., Magnuson, B., Ljungman, M., Park, D., Zhang, C., Campbell, Z. T., Goldstrohm, A. C., & Freddolino, P. L. (2020) · RNA · doi:10.1261/rna.077362.120 · Cited by 22
“Early RIP-Chip 625 experiments with human PUM1 and PUM2 found that genes bound by both proteins belonged to 626 GO terms associated with the Ras pathway, MAPK kinase cascade, PDGF signaling pathway, WNT 627 signaling pathway, small GTPase-mediated signal transduction, and transcription factor activity, 628 among other…”
BackgroundRNA‐binding protein PUM2 regulates mesenchymal stem cell fate via repression of JAK2 and RUNX2 mRNAs
Lee, M., Wu, X.-J., & Zhu, Y. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.29281 · Cited by 28
Yamada, T., Imamachi, N., Imamura, K., Taniue, K., Kawamura, T., Suzuki, Y., Nagahama, M., & Akimitsu, N. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107542 · Cited by 27
Kanitz, A., & Gerber, A. P. (2009) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.55 · Cited by 27
Qiu, C., Bhat, V. D., Rajeev, S., Zhang, C., Lasley, A. E., Wine, R. N., Campbell, Z. T., & Hall, T. M. T. (2019) · eLife · doi:10.7554/elife.48968 · Cited by 26
Maaskola, J., & Rajewsky, N. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1083 · Cited by 27
“The supplementary material of (68) provides a table with log of odds (LOD) scores for binding of PUM1 to genes.”
BackgroundMethodInfluentialVollmeister, E., Haag, C., Zarnack, K., Baumann, S. J., König, J., Mannhaupt, G., & Feldbrügge, M. (2009) · RNA · doi:10.1261/rna.1817609 · Cited by 25
“A significant enrichment for binding sites in the 39 UTR has previously been reported for PUF family RNA-binding proteins (pumilio-Fem-3-binding factor) (Gerber et al. 2004, 2006; Galgano et al. 2008; Morris et al. 2008).”
BackgroundSPIN1 is a proto-oncogene and SPIN3 is a tumor suppressor in human seminoma
Janecki, D. M., Sajek, M. P., Smialek, M. J., Kotecki, M., Ginter-Matuszewska, B., Kuczyńska, B., Spik, A., Kolanowski, T. J., Kitazawa, R., Kurpisz, M. K., et al. (2018) · Oncotarget · doi:10.18632/oncotarget.25977 · Cited by 24
“SPIN1 (also known as SPINDLIN1) was selected as a candidate mRNA target for PUM1 via a RIP-Chip screening of human HeLa cancer cells [10], as it binds Research Paper”
BackgroundMethodInfluentialPumilio1 regulates NPM3/NPM1 axis to promote PD-L1-mediated immune escape in gastric cancer
Wang, H., Zhou, Z., Zhang, J., Hao, T., Wang, P., Su, R., Su, R., Yang, H., Deng, G., Chen, S., et al. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216498 · Cited by 24
Characterization of TgPuf1, a member of the Puf family RNA-binding proteins from Toxoplasma gondii
Liu, M., Miao, J., Liu, T., Sullivan, W. J., Cui, L., & Chen, X. (2014) · Parasites & Vectors · doi:10.1186/1756-3305-7-141 · Cited by 21
“Given the localization of human PUM1 and PUM1 to cytoplasmic stress granules, the punctate staining patterns of TgPuf1 suggest that they might be localized to similar granules, although it still requires co-localization confirmation with a marker for the stress granules or P-bodies [10,44].”
BackgroundLeibovich, L., Mandel‐Gutfreund, Y., & Zohar Yakhini, B. (2010) · Silence · doi:10.1186/1758-907x-1-17 · Cited by 23
“2) We produced a binary vector l(μ) as follows: For each sequence Si in the list of predicted targets for μ, li(μ) = 1 if and only if Si was reported as a Pumilio validated target and also contained the Pumilio consensus motif (UGUAHAUA [25,31]).”
BackgroundMethodInfluentialWang, X., Olson, J., Rasoloson, D., Ellenbecker, M., Bailey, J., & Voronina, E. (2016) · Development · doi:10.1242/dev.140921 · Cited by 23
“For example, rat PUM2 and human PUM1 are found at stress granules, the sites of storage of translationally repressed mRNAs (Morris et al., 2008; Vessey et al., 2006).”
BackgroundEfficient motif search in ranked lists and applications to variable gap motifs
Leibovich, L., & Zohar Yakhini, B. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks206 · Cited by 22
Stress granules (SG) and processing bodies (PB) in viral infections.
Malinowska, M., Niedźwiedzka‐Rystwej, P., Tokarz–Deptuła, B., & Deptuła, W. (2016) · Acta Biochimica Polonica · doi:10.18388/abp.2015_1060 · Cited by 21
“…2003; Tourriere et al., 2003; Baez & Boccacio, 2005; Kedersha et al., 2005; Deigendesh et al., 2006; Kwon et al., 2007; Weissbach & Scadden, 2007; Morris et al., 2008; Anderson & Kedersh, 2008; Onomoto, 2014; Valiente-Echevierria , 2012; Kedrsha et al., 2012; Katoh et al., 2013; White & Lloyd,…”
Wang, X., Ellenbecker, M., Hickey, B., Day, N., Osterli, E., Terzo, M., & Voronina, E. (2020) · eLife · doi:10.7554/elife.52788 · Cited by 18
“elegans, mouse, and human identifying thousands of target mRNAs (Chen et al., 2012; Galgano et al., 2008; Kershner and Kimble, 2010; Morris et al., 2008; Porter et al., 2019; Prasad et al., 2016).”
BackgroundInfluentialPolyadenylation of mRNA as a novel regulatory mechanism of gene expression in temporal lobe epilepsy
Parras, A., de Diego-García, L., Alves, M., Beamer, E. H., Conte, G., Jimenez-Mateos, E. M., Morgan, J., Ollà, I., Hernandez-Santana, Y., Delanty, N., et al. (2020) · Brain · doi:10.1093/brain/awaa168 · Cited by 21
“(2018): 726 associated RNAs identified by RIP-ChIP to human PUM1 in HeLa S3 cells (Morris et al., 2008), 1040 PUM1- and 435 PUM2associated RNAs found by RIP-ChIP to human PUM1 and PUM2 in HeLa S3 cells (Galgano et al.”
Background
Metadata
- Authors
- Morris, A. R., Mukherjee, N., & Keene, J. D.
- Affiliations
- Duke Medical Center (US)
- Corresponding author
- Keene, Jack D.
- ORCID
- Mukherjee, Neelanjan
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 2008-06-01
- Volume
- 28
- Issue
- 12
- Pages
- 4093-4103
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC2423135
- OpenAlex
- W2109821031
- Cited by
- 155
- References
- 62
- Citations by year
- 2026: 6 · 2025: 1 · 2024: 4 · 2023: 2 · 2022: 3 · 2021: 5 · 2020: 10 · 2019: 13 · 2018: 11 · 2017: 7 · 2016: 11 · 2015: 5 · 2014: 12 · 2013: 12 · 2012: 9
- FWCI
- 6.04
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular and Cellular Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (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 › Developmental Biology and Gene Regulation
- Keywords
- PUM1, PUF proteins, mRNA stability, post-transcriptional regulation, 3' untranslated region, cis-regulatory sequences, stress granules, protein synthesis inhibition, ribonucleoprotein, Saccharomyces cerevisiae, Drosophila melanogaster, transcriptional regulation
- MeSH terms
- Animals, Drosophila melanogaster, HeLa Cells, Humans, Models, Biological, Ribosomes, RNA, Messenger, Saccharomyces cerevisiae, Species Specificity, Protein Biosynthesis, RNA-Binding Proteins, Conserved Sequence, Oxidative Stress, Evolution, Molecular, Oligonucleotide Array Sequence Analysis
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
