From Birth to Death: The Complex Lives of Eukaryotic mRNAs

Melissa J. Moore

Abstract: Recent work indicates that the posttranscriptional control of eukaryotic gene expression is much more elaborate and extensive than previously thought, with essentially every step of messenger RNA (mRNA) metabolism being subject to regulation in an mRNA-specific manner. Thus, a comprehensive understanding of eukaryotic gene expression requires an appreciation for how the lives of mRNAs are influenced by a wide array of diverse regulatory mechanisms.

Department of Biochemistry, Howard Hughes Medical Institute, Brandeis University, 415 South Street, Waltham, MA 02454. E-mail: mmoore{at}brandeis.edu

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Protein segregase meddles in remodeling of mRNA-protein complexes.

C.-Y. A. Chen and A.-B. Shyu (2013)
Genes & Dev. 27, 980-984
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The p97-UBXD8 complex destabilizes mRNA by promoting release of ubiquitinated HuR from mRNP.

H.-L. Zhou, C. Geng, G. Luo, and H. Lou (2013)
Genes & Dev. 27, 1046-1058
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The DEAD-box helicase DDX3 substitutes for the cap-binding protein eIF4E to promote compartmentalized translation initiation of the HIV-1 genomic RNA.

R. Soto-Rifo, P. S. Rubilar, and T. Ohlmann (2013)
Nucleic Acids Res.
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Exploring mRNA 3'-UTR G-quadruplexes: evidence of roles in both alternative polyadenylation and mRNA shortening.

J.-D. Beaudoin and J.-P. Perreault (2013)
Nucleic Acids Res.
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EJC core component MLN51 interacts with eIF3 and activates translation.

P.-E. Chazal, E. Daguenet, C. Wendling, N. Ulryck, C. Tomasetto, B. Sargueil, and H. Le Hir (2013)
PNAS 110, 5903-5908
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CDX2 regulation by the RNA-binding protein MEX3A: impact on intestinal differentiation and stemness.

B. Pereira, S. Sousa, R. Barros, L. Carreto, P. Oliveira, C. Oliveira, N. T. Chartier, M. Plateroti, J.-P. Rouault, J.-N. Freund, et al. (2013)
Nucleic Acids Res. 41, 3986-3999
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UV damage regulates alternative polyadenylation of the RPB2 gene in yeast.

L. Yu and M. R. Volkert (2013)
Nucleic Acids Res. 41, 3104-3114
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Antagonistic Function of the RNA-binding Protein HuR and miR-200b in Post-transcriptional Regulation of Vascular Endothelial Growth Factor-A Expression and Angiogenesis.

S.-H. Chang, Y.-C. Lu, X. Li, W.-Y. Hsieh, Y. Xiong, M. Ghosh, T. Evans, O. Elemento, and T. Hla (2013)
J. Biol. Chem. 288, 4908-4921
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Genome-wide Identification and Quantitative Analysis of Cleaved tRNA Fragments Induced by Cellular Stress.

M. Saikia, D. Krokowski, B.-J. Guan, P. Ivanov, M. Parisien, G.-f. Hu, P. Anderson, T. Pan, and M. Hatzoglou (2012)
J. Biol. Chem. 287, 42708-42725
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RNA-binding protein AUF1 represses Dicer expression.

K. Abdelmohsen, K. Tominaga-Yamanaka, S. Srikantan, J.-H. Yoon, M.-J. Kang, and M. Gorospe (2012)
Nucleic Acids Res. 40, 11531-11544
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Human Pumilio Proteins Recruit Multiple Deadenylases to Efficiently Repress Messenger RNAs.

J. Van Etten, T. L. Schagat, J. Hrit, C. A. Weidmann, J. Brumbaugh, J. J. Coon, and A. C. Goldstrohm (2012)
J. Biol. Chem. 287, 36370-36383
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Identifying multi-layer gene regulatory modules from multi-dimensional genomic data.

W. Li, S. Zhang, C.-C. Liu, and X. J. Zhou (2012)
Bioinformatics 28, 2458-2466
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Kinetic signatures of microRNA modes of action.

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RNA 18, 1635-1655
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An in-depth map of polyadenylation sites in cancer.

Y. Lin, Z. Li, F. Ozsolak, S. W. Kim, G. Arango-Argoty, T. T. Liu, S. A. Tenenbaum, T. Bailey, A. P. Monaghan, P. M. Milos, et al. (2012)
Nucleic Acids Res. 40, 8460-8471
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Inverted Alu dsRNA structures do not affect localization but can alter translation efficiency of human mRNAs independent of RNA editing.

C. R. Capshew, K. L. Dusenbury, and H. A. Hundley (2012)
Nucleic Acids Res. 40, 8637-8645
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APOBEC3G Inhibits MicroRNA-mediated Repression of Translation by Interfering with the Interaction between Argonaute-2 and MOV10.

C. Liu, X. Zhang, F. Huang, B. Yang, J. Li, B. Liu, H. Luo, P. Zhang, and H. Zhang (2012)
J. Biol. Chem. 287, 29373-29383
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Up-regulation of miR-1245 by c-myc targets BRCA2 and impairs DNA repair.

L. Song, T. Dai, Y. Xie, C. Wang, C. Lin, Z. Wu, Z. Ying, J. Wu, M. Li, and J. Li (2012)
J Mol Cell Biol 4, 108-117
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The post-transcriptional trans-acting regulator, TbZFP3, co-ordinates transmission-stage enriched mRNAs in Trypanosoma brucei.

P. B. Walrad, P. Capewell, K. Fenn, and K. R. Matthews (2012)
Nucleic Acids Res. 40, 2869-2883
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RNA-binding protein HuR autoregulates its expression by promoting alternative polyadenylation site usage.

W. Dai, G. Zhang, and E. V. Makeyev (2012)
Nucleic Acids Res. 40, 787-800
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Proteomic Analysis of Trichoderma atroviride Reveals Independent Roles for Transcription Factors BLR-1 and BLR-2 in Light and Darkness.

A. Sanchez-Arreguin, A. S. Perez-Martinez, and A. Herrera-Estrella (2012)
Eukaryot. Cell 11, 30-41
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The RNA-Binding Protein Rrm4 is Essential for Efficient Secretion of Endochitinase Cts1.

J. Koepke, F. Kaffarnik, C. Haag, K. Zarnack, N. M. Luscombe, J. Konig, J. Ule, R. Kellner, D. Begerow, and M. Feldbrugge (2011)
Mol. Cell. Proteomics 10, M111.011213
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Export and stability of naturally intronless mRNAs require specific coding region sequences and the TREX mRNA export complex.

H. Lei, A. P. Dias, and R. Reed (2011)
PNAS 108, 17985-17990
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New families of human regulatory RNA structures identified by comparative analysis of vertebrate genomes.

B. J. Parker, I. Moltke, A. Roth, S. Washietl, J. Wen, M. Kellis, R. Breaker, and J. S. Pedersen (2011)
Genome Res. 21, 1929-1943
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Adenosine-to-inosine RNA editing meets cancer.

D. Dominissini, S. Moshitch-Moshkovitz, N. Amariglio, and G. Rechavi (2011)
Carcinogenesis 32, 1569-1577
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Competitive Regulation of Nucleolin Expression by HuR and miR-494.

K. Tominaga, S. Srikantan, E. K. Lee, S. S. Subaran, J. L. Martindale, K. Abdelmohsen, and M. Gorospe (2011)
Mol. Cell. Biol. 31, 4219-4231
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Enhanced translation by Nucleolin via G-rich elements in coding and non-coding regions of target mRNAs.

K. Abdelmohsen, K. Tominaga, E. K. Lee, S. Srikantan, M.-J. Kang, M. M. Kim, R. Selimyan, J. L. Martindale, X. Yang, F. Carrier, et al. (2011)
Nucleic Acids Res. 39, 8513-8530
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A novel function of Tis11b/BRF1 as a regulator of Dll4 mRNA 3'-end processing.

A. Desroches-Castan, N. Cherradi, J.-J. Feige, and D. Ciais (2011)
Mol. Biol. Cell 22, 3625-3633
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Ending the message: poly(A) signals then and now.

N. J. Proudfoot (2011)
Genes & Dev. 25, 1770-1782
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Evolution of Hox Post-Transcriptional Regulation by Alternative Polyadenylation and MicroRNA Modulation Within 12 Drosophila Genomes.

P. Patraquim, M. Warnefors, and C. R. Alonso (2011)
Mol. Biol. Evol. 28, 2453-2460
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Mutation of a C-Terminal Motif Affects Kaposi's Sarcoma-Associated Herpesvirus ORF57 RNA Binding, Nuclear Trafficking, and Multimerization.

A. Taylor, B. R. Jackson, M. Noerenberg, D. J. Hughes, J. R. Boyne, M. Verow, M. Harris, and A. Whitehouse (2011)
J. Virol. 85, 7881-7891
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Control of human {beta}-globin mRNA stability and its impact on beta-thalassemia phenotype.

I. Peixeiro, A. L. Silva, and L. Romao (2011)
Haematologica 96, 905-913
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The Dbp5 cycle at the nuclear pore complex during mRNA export II: nucleotide cycling and mRNP remodeling by Dbp5 are controlled by Nup159 and Gle1.

K. N. Noble, E. J. Tran, A. R. Alcazar-Roman, C. A. Hodge, C. N. Cole, and S. R. Wente (2011)
Genes & Dev. 25, 1065-1077
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Structure-based prediction of RNA-binding domains and RNA-binding sites and application to structural genomics targets.

H. Zhao, Y. Yang, and Y. Zhou (2011)
Nucleic Acids Res. 39, 3017-3025
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Mutations in the RNA Granule Component TDRD7 Cause Cataract and Glaucoma.

S. A. Lachke, F. S. Alkuraya, S. C. Kneeland, T. Ohn, A. Aboukhalil, G. R. Howell, I. Saadi, R. Cavallesco, Y. Yue, A. C.-H. Tsai, et al. (2011)
Science 331, 1571-1576
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Mutation of the 5'-Untranslated Region Stem-Loop Structure Inhibits α1(I) Collagen Expression in Vivo.

C. J. Parsons, B. Stefanovic, E. Seki, T. Aoyama, A. M. Latour, W. F. Marzluff, R. A. Rippe, and D. A. Brenner (2011)
J. Biol. Chem. 286, 8609-8619
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An RNA-zipcode-independent mechanism that localizes Dia1 mRNA to the perinuclear ER through interactions between Dia1 nascent peptide and Rho-GTP.

G. Liao, X. Ma, and G. Liu (2011)
J. Cell Sci. 124, 589-599
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The Regulation of Parathyroid Hormone Secretion and Synthesis.

R. Kumar and J. R. Thompson (2011)
J. Am. Soc. Nephrol. 22, 216-224
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A link between nuclear RNA surveillance, the human exosome and RNA polymerase II transcriptional termination.

S. F. de Almeida, A. Garcia-Sacristan, N. Custodio, and M. Carmo-Fonseca (2010)
Nucleic Acids Res. 38, 8015-8026
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Polyamines Regulate the Stability of JunD mRNA by Modulating the Competitive Binding of Its 3' Untranslated Region to HuR and AUF1.

T. Zou, J. N. Rao, L. Liu, L. Xiao, T.-X. Yu, P. Jiang, M. Gorospe, and J.-Y. Wang (2010)
Mol. Cell. Biol. 30, 5021-5032
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Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules.

D. A. Bosco, N. Lemay, H. K. Ko, H. Zhou, C. Burke, T. J. Kwiatkowski Jr, P. Sapp, D. McKenna-Yasek, R. H. Brown Jr, and L. J. Hayward (2010)
Hum. Mol. Genet. 19, 4160-4175
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Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function.

M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner (2010)
PNAS 107, 17864-17871
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Characterization of EMU, the Arabidopsis homolog of the yeast THO complex member HPR1.

C. Furumizu, H. Tsukaya, and Y. Komeda (2010)
RNA 16, 1809-1817
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Developmental RNA processing of 3'UTRs in Hox mRNAs as a context-dependent mechanism modulating visibility to microRNAs.

S. Thomsen, G. Azzam, R. Kaschula, L. S. Williams, and C. R. Alonso (2010)
Development 137, 2951-2960
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Recognition of Polyadenosine RNA by the Zinc Finger Domain of Nuclear Poly(A) RNA-binding Protein 2 (Nab2) Is Required for Correct mRNA 3'-End Formation.

S. M. Kelly, S. W. Leung, L. H. Apponi, A. M. Bramley, E. J. Tran, J. A. Chekanova, S. R. Wente, and A. H. Corbett (2010)
J. Biol. Chem. 285, 26022-26032
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Human G3BP1 interacts with {beta}-F1-ATPase mRNA and inhibits its translation.

A. D. Ortega, I. M. Willers, S. Sala, and J. M. Cuezva (2010)
J. Cell Sci. 123, 2685-2696
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Effect of pulmonary rehabilitation on muscle remodelling in cachectic patients with COPD.

I. Vogiatzis, D. C. M. Simoes, G. Stratakos, E. Kourepini, G. Terzis, P. Manta, D. Athanasopoulos, C. Roussos, P. D. Wagner, and S. Zakynthinos (2010)
Eur. Respir. J. 36, 301-310
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SRp40 and SRp55 Promote the Translation of Unspliced Human Immunodeficiency Virus Type 1 RNA.

C. M. Swanson, N. M. Sherer, and M. H. Malim (2010)
J. Virol. 84, 6748-6759
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A Review of Methods to Monitor the Modulation of mRNA Stability: A Novel Approach to Drug Discovery and Therapeutic Intervention.

D. Cheneval, T. Kastelic, P. Fuerst, and C. N. Parker (2010)
J Biomol Screen 15, 609-622
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Structural and functional analysis of the interaction between the nucleoporin Nup98 and the mRNA export factor Rae1.

Y. Ren, H.-S. Seo, G. Blobel, and A. Hoelz (2010)
PNAS 107, 10406-10411
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The life of an mRNA in space and time.

Y. Ben-Ari, Y. Brody, N. Kinor, A. Mor, T. Tsukamoto, D. L. Spector, R. H. Singer, and Y. Shav-Tal (2010)
J. Cell Sci. 123, 1761-1774
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Minireview: Global Regulation and Dynamics of Ribonucleic Acid.

J. D. Keene (2010)
Endocrinology 151, 1391-1397
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Minireview: Posttranscriptional Regulation of the Insulin and Insulin-Like Growth Factor Systems.

E. K. Lee and M. Gorospe (2010)
Endocrinology 151, 1403-1408
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Stress granule formation mediates the inhibition of colonic Hsp70 translation by interferon-{gamma} and tumor necrosis factor-{alpha}.

S. Hu, E. C. Claud, M. W. Musch, and E. B. Chang (2010)
Am J Physiol Gastrointest Liver Physiol 298, G481-G492
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Tandem Phosphorylation of Serines 221 and 318 by Protein Kinase C{delta} Coordinates mRNA Binding and Nucleocytoplasmic Shuttling of HuR.

A. Doller, K. Schlepckow, H. Schwalbe, J. Pfeilschifter, and W. Eberhardt (2010)
Mol. Cell. Biol. 30, 1397-1410
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A global comparison between nuclear and cytosolic transcriptomes reveals differential compartmentalization of alternative transcript isoforms.

L. Chen (2010)
Nucleic Acids Res. 38, 1086-1097
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Nonsense-Mediated RNA Decay Regulation by Cellular Stress: Implications for Tumorigenesis.

L. B. Gardner (2010)
Mol. Cancer Res. 8, 295-308
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An unexpected ending: Noncanonical 3' end processing mechanisms.

J. E. Wilusz and D. L. Spector (2010)
RNA 16, 259-266
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NF90 selectively represses the translation of target mRNAs bearing an AU-rich signature motif.

Y. Kuwano, R. Pullmann Jr., B. S. Marasa, K. Abdelmohsen, E. K. Lee, X. Yang, J. L. Martindale, M. Zhan, and M. Gorospe (2010)
Nucleic Acids Res. 38, 225-238
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Role of Microtubules in Stress Granule Assembly: MICROTUBULE DYNAMICAL INSTABILITY FAVORS THE FORMATION OF MICROMETRIC STRESS GRANULES IN CELLS.

K. G. Chernov, A. Barbet, L. Hamon, L. P. Ovchinnikov, P. A. Curmi, and D. Pastre (2009)
J. Biol. Chem. 284, 36569-36580
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Mammalian pre-mRNA 3' End Processing Factor CF Im68 Functions in mRNA Export.

M.-D. Ruepp, C. Aringhieri, S. Vivarelli, S. Cardinale, S. Paro, D. Schumperli, and S. M.L. Barabino (2009)
Mol. Biol. Cell 20, 5211-5223
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Stabilization of XIAP mRNA through the RNA binding protein HuR regulated by cellular polyamines.

X. Zhang, T. Zou, J. N. Rao, L. Liu, L. Xiao, P.-Y. Wang, Y.-H. Cui, M. Gorospe, and J.-Y. Wang (2009)
Nucleic Acids Res. 37, 7623-7637
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Tandem KH domains of Khd4 recognize AUACCC and are essential for regulation of morphology as well as pathogenicity in Ustilago maydis.

E. Vollmeister, C. Haag, K. Zarnack, S. Baumann, J. Konig, G. Mannhaupt, and M. Feldbrugge (2009)
RNA 15, 2206-2218
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IGF2 mRNA-binding protein 2: biological function and putative role in type 2 diabetes.

J. Christiansen, A. M Kolte, T. v O Hansen, and F. C Nielsen (2009)
J. Mol. Endocrinol. 43, 187-195
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Role for Kruppel-Like Factor 4 in Determining the Outcome of p53 Response to DNA Damage.

Q. Zhou, Y. Hong, Q. Zhan, Y. Shen, and Z. Liu (2009)
Cancer Res. 69, 8284-8292
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Increased MKK4 Abundance with Replicative Senescence Is Linked to the Joint Reduction of Multiple MicroRNAs.

B. S. Marasa, S. Srikantan, K. Masuda, K. Abdelmohsen, Y. Kuwano, X. Yang, J. L. Martindale, C. W. Rinker-Schaeffer, and M. Gorospe (2009)
Science Signaling 2, ra69
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Drosophila Suppressor of Sable Protein [Su(s)] Promotes Degradation of Aberrant and Transposon-Derived RNAs.

Y.-S. Kuan, P. Brewer-Jensen, W.-L. Bai, C. Hunter, C. B. Wilson, S. Bass, J. Abernethy, J. S. Wing, and L. L. Searles (2009)
Mol. Cell. Biol. 29, 5590-5603
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IL-8 Regulates Mucin Gene Expression at the Posttranscriptional Level in Lung Epithelial Cells.

M. V. Bautista, Y. Chen, V. S. Ivanova, M. K. Rahimi, A. M. Watson, and M. C. Rose (2009)
J. Immunol. 183, 2159-2166
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HuR recruits let-7/RISC to repress c-Myc expression.

H. H. Kim, Y. Kuwano, S. Srikantan, E. K. Lee, J. L. Martindale, and M. Gorospe (2009)
Genes & Dev. 23, 1743-1748
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Cotranscriptional recruitment of the nuclear poly(A)-binding protein Pab2 to nascent transcripts and association with translating mRNPs.

C. Lemieux and F. Bachand (2009)
Nucleic Acids Res. 37, 3418-3430
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Heterogeneous Nuclear Ribonucleoprotein G Regulates Splice Site Selection by Binding to CC(A/C)-rich Regions in Pre-mRNA.

B. Heinrich, Z. Zhang, O. Raitskin, M. Hiller, N. Benderska, A. M. Hartmann, L. Bracco, D. Elliott, S. Ben-Ari, H. Soreq, et al. (2009)
J. Biol. Chem. 284, 14303-14315
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Thoc1 Deficiency Compromises Gene Expression Necessary for Normal Testis Development in the Mouse.

X. Wang, M. Chinnam, J. Wang, Y. Wang, X. Zhang, E. Marcon, P. Moens, and D. W. Goodrich (2009)
Mol. Cell. Biol. 29, 2794-2803
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Studying membrane proteins through the eyes of the genetic code revealed a strong uracil bias in their coding mRNAs.

J. Prilusky and E. Bibi (2009)
PNAS 106, 6662-6666
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A highly conserved cis-regulatory motif directs differential gonadal synexpression of Dmrt1 transcripts during gonad development.

A. Herpin, S. Nakamura, T. U. Wagner, M. Tanaka, and M. Schartl (2009)
Nucleic Acids Res. 37, 1510-1520
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cAMP-Dependent Posttranscriptional Regulation of Steroidogenic Acute Regulatory (STAR) Protein by the Zinc Finger Protein ZFP36L1/TIS11b.

H. Duan, N. Cherradi, J.-J. Feige, and C. Jefcoate (2009)
Mol. Endocrinol. 23, 497-509
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Similar Regulation of Human Inducible Nitric-oxide Synthase Expression by Different Isoforms of the RNA-binding Protein AUF1.

A. Pautz, K. Linker, S. Altenhofer, S. Heil, N. Schmidt, J. Art, S. Knauer, R. Stauber, N. Sadri, A. Pont, et al. (2009)
J. Biol. Chem. 284, 2755-2766
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A Universal Nonmonotonic Relationship between Gene Compactness and Expression Levels in Multicellular Eukaryotes.

L. Carmel and E. V. Koonin (2009)
Genome Biol Evol 1, 382-390
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Conservation of the Protein Composition and Electron Microscopy Structure of Drosophila melanogaster and Human Spliceosomal Complexes.

N. Herold, C. L. Will, E. Wolf, B. Kastner, H. Urlaub, and R. Luhrmann (2009)
Mol. Cell. Biol. 29, 281-301
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Identification of a signature motif in target mRNAs of RNA-binding protein AUF1.

K. Mazan-Mamczarz, Y. Kuwano, M. Zhan, E. J. White, J. L. Martindale, A. Lal, and M. Gorospe (2009)
Nucleic Acids Res. 37, 204-214
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The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo.

J. E. Bestman and H. T. Cline (2008)
PNAS 105, 20494-20499
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miR-519 reduces cell proliferation by lowering RNA-binding protein HuR levels.

K. Abdelmohsen, S. Srikantan, Y. Kuwano, and M. Gorospe (2008)
PNAS 105, 20297-20302
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