Roquin promotes constitutive mrna decay via a conserved class of stem-loop recognition motifs

Cell

Volumn 153, Issue 4, 2013, Pages 869-881

  Leppek, Kathrin ^a   Schott, Johanna ^a   Reitter, Sonja ^a   Poetz, Fabian ^a   Hammond, Ming C ^b   Stoecklin, Georg ^a  

^a GERMAN CANCER RESEARCH CENTER   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN DERIVATIVE; ROQUIN; TRANSCRIPTOME; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FOLDING; RNA DEGRADATION; RNA STRUCTURE;

EID: 84877708543     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.04.016     Document Type: Article

References (45)

1. A. Androulidaki, D. Iliopoulos, A. Arranz, C. Doxaki, S. Schworer, V. Zacharioudaki, A.N. Margioris, P.N. Tsichlis, and C. Tsatsanis The kinase Akt1 controls macrophage response to lipopolysaccharide by regulating microRNAs Immunity 31 2009 220 231
2. A. Arlt, and H. Schäfer Role of the immediate early response 3 (IER3) gene in cellular stress response, inflammation and tumorigenesis Eur. J. Cell Biol. 90 2011 545 552
3. V. Athanasopoulos, A. Barker, D. Yu, A.H. Tan, M. Srivastava, N. Contreras, J. Wang, K.P. Lam, S.H. Brown, and C.C. Goodnow The ROQUIN family of proteins localizes to stress granules via the ROQ domain and binds target mRNAs FEBS J. 277 2010 2109 2127
4. A. Bertossi, M. Aichinger, P. Sansonetti, M. Lech, F. Neff, M. Pal, F.T. Wunderlich, H.J. Anders, L. Klein, and M. Schmidt-Supprian Loss of Roquin induces early death and immune deregulation but not autoimmunity J. Exp. Med. 208 2011 1749 1756
5. J.R. Bradley TNF-mediated inflammatory disease J. Pathol. 214 2008 149 160
6. E. Carballo, W.S. Lai, and P.J. Blackshear Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin Science 281 1998 1001 1005
7. C.Y. Chen, R. Gherzi, S.E. Ong, E.L. Chan, R. Raijmakers, G.J. Pruijn, G. Stoecklin, C. Moroni, M. Mann, and M. Karin AU binding proteins recruit the exosome to degrade ARE-containing mRNAs Cell 107 2001 451 464
8. M.A. Collart, and O.O. Panasenko The Ccr4 - not complex Gene 492 2012 42 53
9. M. Fenger-Grøn, C. Fillman, B. Norrild, and J. Lykke-Andersen Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping Mol. Cell 20 2005 905 915
10. N.L. Garneau, J. Wilusz, and C.J. Wilusz The highways and byways of mRNA decay Nat. Rev. Mol. Cell Biol. 8 2007 113 126
11. E. Glasmacher, K.P. Hoefig, K.U. Vogel, N. Rath, L. Du, C. Wolf, E. Kremmer, X. Wang, and V. Heissmeyer Roquin binds inducible costimulator mRNA and effectors of mRNA decay to induce microRNA-independent post-transcriptional repression Nat. Immunol. 11 2010 725 733
12. H. Goodarzi, H.S. Najafabadi, P. Oikonomou, T.M. Greco, L. Fish, R. Salavati, I.M. Cristea, and S. Tavazoie Systematic discovery of structural elements governing stability of mammalian messenger RNAs Nature 485 2012 264 268
13. S. Hao, and D. Baltimore The stability of mRNA influences the temporal order of the induction of genes encoding inflammatory molecules Nat. Immunol. 10 2009 281 288
14. E. Huntzinger, and E. Izaurralde Gene silencing by microRNAs: contributions of translational repression and mRNA decay Nat. Rev. Genet. 12 2011 99 110
15. Y.R. Ji, H.J. Kim, D.H. Yu, K.B. Bae, S.J. Park, J.K. Yi, N. Kim, S.J. Park, K.B. Oh, and S.S. Hwang Enforced expression of roquin protein in T cells exacerbates the incidence and severity of experimental arthritis J. Biol. Chem. 287 2012 42269 42277
16. W.F. Marzluff, E.J. Wagner, and R.J. Duronio Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail Nat. Rev. Genet. 9 2008 843 854
17. K. Matsushita, O. Takeuchi, D.M. Standley, Y. Kumagai, T. Kawagoe, T. Miyake, T. Satoh, H. Kato, T. Tsujimura, H. Nakamura, and S. Akira Zc3h12a is an RNase essential for controlling immune responses by regulating mRNA decay Nature 458 2009 1185 1190
18. B.J. Parker, I. Moltke, A. Roth, S. Washietl, J. Wen, M. Kellis, R. Breaker, and J.S. Pedersen New families of human regulatory RNA structures identified by comparative analysis of vertebrate genomes Genome Res. 21 2011 1929 1943
19. M. Rabani, J.Z. Levin, L. Fan, X. Adiconis, R. Raychowdhury, M. Garber, A. Gnirke, C. Nusbaum, N. Hacohen, and N. Friedman Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells Nat. Biotechnol. 29 2011 436 442
20. F. Renner, and M.L. Schmitz Autoregulatory feedback loops terminating the NF-kappaB response Trends Biochem. Sci. 34 2009 128 135
21. H. Sandler, J. Kreth, H.T. Timmers, and G. Stoecklin Not1 mediates recruitment of the deadenylase Caf1 to mRNAs targeted for degradation by tristetraprolin Nucleic Acids Res. 39 2011 4373 4386
22. B. Schwanhäusser, D. Busse, N. Li, G. Dittmar, J. Schuchhardt, J. Wolf, W. Chen, and M. Selbach Global quantification of mammalian gene expression control Nature 473 2011 337 342
23. Z. Shu, and P.C. Bevilacqua Isolation and characterization of thermodynamically stable and unstable RNA hairpins from a triloop combinatorial library Biochemistry 38 1999 15369 15379
24. C. Srisawat, and D.R. Engelke Streptavidin aptamers: affinity tags for the study of RNAs and ribonucleoproteins RNA 7 2001 632 641
25. G. Stoecklin, M. Lu, B. Rattenbacher, and C. Moroni A constitutive decay element promotes tumor necrosis factor alpha mRNA degradation via an AU-rich element-independent pathway Mol. Cell. Biol. 23 2003 3506 3515
26. K.J. Tracey, and A. Cerami Tumor necrosis factor: a pleiotropic cytokine and therapeutic target Annu. Rev. Med. 45 1994 491 503
27. C.G. Vinuesa, M.C. Cook, C. Angelucci, V. Athanasopoulos, L. Rui, K.M. Hill, D. Yu, H. Domaschenz, B. Whittle, and T. Lambe A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity Nature 435 2005 452 458
28. D. Yu, A.H. Tan, X. Hu, V. Athanasopoulos, N. Simpson, D.G. Silva, A. Hutloff, K.M. Giles, P.J. Leedman, and K.P. Lam Roquin represses autoimmunity by limiting inducible T-cell co-stimulator messenger RNA Nature 450 2007 299 303
29. S. Anders, and W. Huber Differential expression analysis for sequence count data Genome Biol. 11 2010 R106
30. D. Blankenberg, J. Taylor, A. Nekrutenko Galaxy Team Making whole genome multiple alignments usable for biologists Bioinformatics 27 2011 2426 2428
31. E.I. Boyle, S. Weng, J. Gollub, H. Jin, D. Botstein, J.M. Cherry, and G. Sherlock GO:TermFinder - open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes Bioinformatics 20 2004 3710 3715
32. D. Charif, and J.R. Lobry SeqinR 1.0-2: a contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis U. Bastolla, M. Porto, H.E. Roman, M. Vendruscolo, Structural Approaches to Sequence Evolution: Molecules, Networks, Populations (Biological and Medical Physics, Biomedical Engineering) 2007 Springer Verlag Berlin, Heidelberg, Germany 207 232
33. N. Delhomme, I. Padioleau, E.E. Furlong, and L.M. Steinmetz easyRNASeq: a bioconductor package for processing RNA-Seq data Bioinformatics 28 2012 2532 2533
34. P.A. Fujita, B. Rhead, A.S. Zweig, A.S. Hinrichs, D. Karolchik, M.S. Cline, M. Goldman, G.P. Barber, H. Clawson, and A. Coelho The UCSC Genome Browser database: update 2011 Nucleic Acids Res. 39 Database issue 2011 D876 D882
35. H. Li, and R. Durbin Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 25 2009 1754 1760
36. S. Niranjanakumari, E. Lasda, R. Brazas, and M.A. Garcia-Blanco Reversible cross-linking combined with immunoprecipitation to study RNA-protein interactions in vivo Methods 26 2002 182 190
37. S. Ozgur, M. Chekulaeva, and G. Stoecklin Human Pat1b connects deadenylation with mRNA decapping and controls the assembly of processing bodies Mol. Cell. Biol. 30 2010 4308 4323
38. E.E. Regulski, and R.R. Breaker In-line probing analysis of riboswitches Methods Mol. Biol. 419 2008 53 67
39. U. Rothbauer, K. Zolghadr, S. Muyldermans, A. Schepers, M.C. Cardoso, and H. Leonhardt A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins Mol. Cell. Proteomics 7 2008 282 289
40. S.P. Ryder, M.I. Recht, and J.R. Williamson Quantitative analysis of protein-RNA interactions by gel mobility shift Methods Mol. Biol. 488 2008 99 115
41. G. Stoecklin, P. Stoeckle, M. Lu, O. Muehlemann, and C. Moroni Cellular mutants define a common mRNA degradation pathway targeting cytokine AU-rich elements RNA 7 2001 1578 1588
42. G. Stoecklin, B. Gross, X.F. Ming, and C. Moroni A novel mechanism of tumor suppression by destabilizing AU-rich growth factor mRNA Oncogene 22 2003 3554 3561
43. G. Stoecklin, S.A. Tenenbaum, T. Mayo, S.V. Chittur, A.D. George, T.E. Baroni, P.J. Blackshear, and P. Anderson Genome-wide analysis identifies interleukin-10 mRNA as target of tristetraprolin J. Biol. Chem. 283 2008 11689 11699
44. G.S. Winkler, K.W. Mulder, V.J. Bardwell, E. Kalkhoven, and H.T. Timmers Human Ccr4-Not complex is a ligand-dependent repressor of nuclear receptor-mediated transcription EMBO J. 25 2006 3089 3099
45. N. Xu, P. Loflin, C.Y. Chen, and A.B. Shyu A broader role for AU-rich element-mediated mRNA turnover revealed by a new transcriptional pulse strategy Nucleic Acids Res. 26 1998 558 565