Regnase-1 and roquin regulate a common element in inflammatory mRNAs by spatiotemporally distinct mechanisms

Cell

Volumn 161, Issue 5, 2015, Pages 1058-1073

  Mino, Takashi ^a,b   Murakawa, Yasuhiro ^c   Fukao, Akira ^d,i   Vandenbon, Alexis ^e   Wessels, Hans Hermann ^c   Ori, Daisuke ^a,b   Uehata, Takuya ^a   Tartey, Sarang ^a,b   Akira, Shizuo ^e,f   Suzuki, Yutaka ^g   Vinuesa, Carola G ^h   Ohler, Uwe ^c   Standley, Daron M ^a,e   Landthaler, Markus ^c   Fujiwara, Toshinobu ^d   Takeuchi, Osamu ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d NAGOYA CITY UNIVERSITY   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f OSAKA UNIVERSITY   (Japan)

^g UNIVERSITY OF TOKYO   (Japan)

^h Australian National University   (Australia)

ⁱ KINKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; MESSENGER RNA; PROTEIN; REGNASE 1 PROTEIN; ROQUIN PROTEIN; UNCLASSIFIED DRUG; RC3H1 PROTEIN, MOUSE; RENT1 PROTEIN, MOUSE; RIBONUCLEASE; RIBOSOME PROTEIN; STOP CODON; TRANSACTIVATOR PROTEIN; UBIQUITIN PROTEIN LIGASE; ZC3H12A PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL GRANULE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; FIBROBLAST; IMMUNOREGULATION; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; RIBOSOME; SPATIOTEMPORAL ANALYSIS; STOP CODON; 3T3 CELL LINE; ANIMAL; CHEMISTRY; CONFORMATION; GENETICS; HELA CELL LINE; HUMAN; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POLYSOME; PROTEIN SYNTHESIS; RNA STABILITY;

ANIMALS; BASE SEQUENCE; CODON, TERMINATOR; HELA CELLS; HUMANS; INFLAMMATION; MICE; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; NUCLEIC ACID CONFORMATION; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; RIBONUCLEASES; RIBOSOMAL PROTEINS; RNA STABILITY; RNA, MESSENGER; TRANS-ACTIVATORS; UBIQUITIN-PROTEIN LIGASES;

EID: 84930221877     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.04.029     Document Type: Article

References (36)

1. P. Anderson Post-transcriptional regulons coordinate the initiation and resolution of inflammation Nat. Rev. Immunol. 10 2010 24 35
2. P. Anderson, and N. Kedersha RNA granules: post-transcriptional and epigenetic modulators of gene expression Nat. Rev. Mol. Cell Biol. 10 2009 430 436
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. V. Balagopal, and R. Parker Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs Curr. Opin. Cell Biol. 21 2009 403 408
5. R. Chovatiya, and R. Medzhitov Stress, inflammation, and defense of homeostasis Mol. Cell 54 2014 281 288
6. M.K. Doma, and R. Parker Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation Nature 440 2006 561 564
7. A.B. Eberle, S. Lykke-Andersen, O. Mühlemann, and T.H. Jensen SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells Nat. Struct. Mol. Biol. 16 2009 49 55
8. T.M. Franks, G. Singh, and J. Lykke-Andersen Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense- mediated mRNA decay Cell 143 2010 938 950
9. J.R. Hogg, and S.P. Goff Upf1 senses 3'UTR length to potentiate mRNA decay Cell 143 2010 379 389
10. J.A. Hurt, A.D. Robertson, and C.B. Burge Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay Genome Res. 23 2013 1636 1650
11. H. Iwasaki, O. Takeuchi, S. Teraguchi, K. Matsushita, T. Uehata, K. Kuniyoshi, T. Satoh, T. Saitoh, M. Matsushita, D.M. Standley, and S. Akira The IκB kinase complex regulates the stability of cytokine-encoding mRNA induced by TLR-IL-1R by controlling degradation of regnase-1 Nat. Immunol. 12 2011 1167 1175
12. K.M. Jeltsch, D. Hu, S. Brenner, J. Zöller, G.A. Heinz, D. Nagel, K.U. Vogel, N. Rehage, S.C. Warth, and S.L. Edelmann Cleavage of roquin and regnase-1 by the paracaspase MALT1 releases their cooperatively repressed targets to promote T(H)17 differentiation Nat. Immunol. 15 2014 1079 1089
13. P. Kafasla, A. Skliris, and D.L. Kontoyiannis Post-transcriptional coordination of immunological responses by RNA-binding proteins Nat. Immunol. 15 2014 492 502
14. H. Kaygun, and W.F. Marzluff Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1 Nat. Struct. Mol. Biol. 12 2005 794 800
15. S. Kervestin, and A. Jacobson NMD: a multifaceted response to premature translational termination Nat. Rev. Mol. Cell Biol. 13 2012 700 712
16. Y.K. Kim, L. Furic, L. Desgroseillers, and L.E. Maquat Mammalian Staufen1 recruits Upf1 to specific mRNA 3'UTRs so as to elicit mRNA decay Cell 120 2005 195 208
17. T. Kurosaki, and L.E. Maquat Rules that govern UPF1 binding to mRNA 3′ UTRs Proc. Natl. Acad. Sci. USA 110 2013 3357 3362
18. K. Leppek, J. Schott, S. Reitter, F. Poetz, M.C. Hammond, and G. Stoecklin Roquin promotes constitutive mRNA decay via a conserved class of stem-loop recognition motifs Cell 153 2013 869 881
19. M.A. Linterman, R.J. Rigby, R.K. Wong, D. Yu, R. Brink, J.L. Cannons, P.L. Schwartzberg, M.C. Cook, G.D. Walters, and C.G. Vinuesa Follicular helper T cells are required for systemic autoimmunity J. Exp. Med. 206 2009 561 576
20. B. Loh, S. Jonas, and E. Izaurralde The SMG5-SMG7 heterodimer directly recruits the CCR4-NOT deadenylase complex to mRNAs containing nonsense codons via interaction with POP2 Genes Dev. 27 2013 2125 2138
21. 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
22. E.M. Moresco, D. LaVine, and B. Beutler Toll-like receptors Curr. Biol. 21 2011 R488 R493
23. E. Park, M.L. Gleghorn, and L.E. Maquat Staufen2 functions in Staufen1-mediated mRNA decay by binding to itself and its paralog and promoting UPF1 helicase but not ATPase activity Proc. Natl. Acad. Sci. USA 110 2013 405 412
24. M.W. Popp, and L.E. Maquat Organizing principles of mammalian nonsense-mediated mRNA decay Annu. Rev. Genet. 47 2013 139 165
25. A. Pratama, R.R. Ramiscal, D.G. Silva, S.K. Das, V. Athanasopoulos, J. Fitch, N.K. Botelho, P.P. Chang, X. Hu, and J.J. Hogan Roquin-2 shares functions with its paralog Roquin-1 in the repression of mRNAs controlling T follicular helper cells and systemic inflammation Immunity 38 2013 669 680
26. A. Schlundt, G.A. Heinz, R. Janowski, A. Geerlof, R. Stehle, V. Heissmeyer, D. Niessing, and M. Sattler Structural basis for RNA recognition in roquin-mediated post-transcriptional gene regulation Nat. Struct. Mol. Biol. 21 2014 671 678
27. A. Schuetz, Y. Murakawa, E. Rosenbaum, M. Landthaler, and U. Heinemann Roquin binding to target mRNAs involves a winged helix-turn-helix motif Nat. Commun. 5 2014 5701
28. C. Schweingruber, S.C. Rufener, D. Zünd, A. Yamashita, and O. Mühlemann Nonsense-mediated mRNA decay - mechanisms of substrate mRNA recognition and degradation in mammalian cells Biochim. Biophys. Acta 1829 2013 612 623
29. H.I. Suzuki, M. Arase, H. Matsuyama, Y.L. Choi, T. Ueno, H. Mano, K. Sugimoto, and K. Miyazono MCPIP1 ribonuclease antagonizes dicer and terminates microRNA biogenesis through precursor microRNA degradation Mol. Cell 44 2011 424 436
30. O. Takeuchi, and S. Akira Pattern recognition receptors and inflammation Cell 140 2010 805 820
31. D. Tan, M. Zhou, M. Kiledjian, and L. Tong The ROQ domain of Roquin recognizes mRNA constitutive-decay element and double-stranded RNA Nat. Struct. Mol. Biol. 21 2014 679 685
32. T. Uehata, H. Iwasaki, A. Vandenbon, K. Matsushita, E. Hernandez-Cuellar, K. Kuniyoshi, T. Satoh, T. Mino, Y. Suzuki, and D.M. Standley Malt1-induced cleavage of regnase-1 in CD4(+) helper T cells regulates immune activation Cell 153 2013 1036 1049
33. 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
34. K.U. Vogel, S.L. Edelmann, K.M. Jeltsch, A. Bertossi, K. Heger, G.A. Heinz, J. Zöller, S.C. Warth, K.P. Hoefig, and C. Lohs Roquin paralogs 1 and 2 redundantly repress the Icos and Ox40 costimulator mRNAs and control follicular helper T cell differentiation Immunity 38 2013 655 668
35. 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
36. D. Zünd, A.R. Gruber, M. Zavolan, and O. Mühlemann Translation-dependent displacement of UPF1 from coding sequences causes its enrichment in 3′ UTRs Nat. Struct. Mol. Biol. 20 2013 936 943