A conformational RNA zipper promotes intron ejection during non-conventional XBP1 mRNA splicing

EMBO Reports

Volumn 16, Issue 12, 2015, Pages 1688-1698

  Peschek, Jirka ^a   Acosta Alvear, Diego ^a   Mendez, Aaron S ^a,b   Walter, Peter ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

endoribonuclease; ER stress; RNA conformational change; unfolded protein response; XBP1 splicing

Indexed keywords

MESSENGER RNA; X BOX BINDING PROTEIN 1; DNA BINDING PROTEIN; ERN1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; REGULATORY FACTOR X TRANSCRIPTION FACTOR; RIBONUCLEASE; TRANSCRIPTION FACTOR; XBP1 PROTEIN, HUMAN;

ARTICLE; CLINICAL FEATURE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EXON; GENE REARRANGEMENT; HUMAN; IN VIVO STUDY; INTRON; NONHUMAN; PRIORITY JOURNAL; RNA CONFORMATION; RNA PROCESSING; RNA SPLICING; ANIMAL; CONFORMATION; CONSERVED SEQUENCE; DNA SEQUENCE; ENDOPLASMIC RETICULUM; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN FOLDING; SEQUENCE ALIGNMENT; UNFOLDED PROTEIN RESPONSE;

ANIMALS; BASE SEQUENCE; CONSERVED SEQUENCE; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; HUMANS; INTRONS; NUCLEIC ACID CONFORMATION; PROTEIN FOLDING; PROTEIN-SERINE-THREONINE KINASES; REGULATORY FACTOR X TRANSCRIPTION FACTORS; RNA SPLICING; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UNFOLDED PROTEIN RESPONSE; X-BOX BINDING PROTEIN 1;

EID: 84954360595     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201540955     Document Type: Article

References (39)

1. Walter P, Ron D, (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334: 1081-1086
2. Ron D, Walter P, (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529
3. Haze K, Yoshida H, Yanagi H, Yura T, Mori K, (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10: 3787-3799
4. Harding HP, Zhang Y, Ron D, (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274
5. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D, (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96
6. Shen X, Ellis RE, Lee K, Liu C-Y, Yang K, Solomon A, Yoshida H, Morimoto R, Kurnit DM, Mori K, et al, (2001) Complementary signaling pathways regulate the unfolded protein response and are required for C. Elegans development. Cell 107: 893-903
7. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K, (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891
8. Korennykh AV, Egea PF, Korostelev AA, Finer-Moore J, Zhang C, Shokat KM, Stroud RM, Walter P, (2009) The unfolded protein response signals through high-order assembly of Ire1. Nature 457: 687-693
9. Korennykh A, Walter P, (2012) Structural basis of the unfolded protein response. Annu Rev Cell Dev Biol 28: 251-277
10. Kawahara T, Yanagi H, Yura T, Mori K, (1998) Unconventional splicing of HAC1/ERN4 mRNA required for the unfolded protein response sequence-specific and non-sequential cleavage of the splice sites. J Biol Chem 273: 1802-1807
11. Cox JS, Walter P, (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87: 391-404
12. Sidrauski C, Cox JS, Walter P, (1996) tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell 87: 405-413
13. Jurkin J, Henkel T, Nielsen AF, Minnich M, Popow J, Kaufmann T, Heindl K, Hoffmann T, Busslinger M, Martinez J, (2014) The mammalian tRNA ligase complex mediates splicing of XBP1 mRNA and controls antibody secretion in plasma cells. EMBO J 33: 2922-2936
14. Kosmaczewski SG, Edwards TJ, Han SM, Eckwahl MJ, Meyer BI, Peach S, Hesselberth JR, Wolin SL, Hammarlund M, (2014) The RtcB RNA ligase is an essential component of the metazoan unfolded protein response. EMBO Rep 15: 1278-1285
15. u Y, Liang F-X, Wang X, (2014) A synthetic biology approach identifies the mammalian UPR RNA ligase RtcB. Mol Cell 55: 758-770
16. Acosta-Alvear D, Zhou Y, Blais A, Tsikitis M, Lents NH, Arias C, Lennon CJ, Kluger Y, Dynlacht BD, (2007) XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol Cell 27: 53-66
17. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P, (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249-258
18. Hollien J, Weissman JS, (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313: 104-107
19. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS, (2009) Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186: 323-331
20. Hooks KB, Griffiths-Jones S, (2011) Conserved RNA structures in the non-canonical Hac1/Xbp1 intron. RNA Biol 8: 552-556
21. Korennykh AV, Korostelev AA, Egea PF, Finer-Moore J, Stroud RM, Zhang C, Shokat KM, Walter P, (2011) Structural and functional basis for RNA cleavage by Ire1. BMC Biol 9: 47
22. Kertesz M, Wan Y, Mazor E, Rinn JL, Nutter RC, Chang HY, Segal E, (2010) Genome-wide measurement of RNA secondary structure in yeast. Nature 467: 103-107
23. Wan Y, Qu K, Zhang QC, Flynn RA, Manor O, Ouyang Z, Zhang J, Spitale RC, Snyder MP, Segal E, et al, (2014) Landscape and variation of RNA secondary structure across the human transcriptome. Nature 505: 706-709
24. Gonzalez TN, Sidrauski C, Dörfler S, Walter P, (1999) Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway. EMBO J 18: 3119-3132
25. Greer CL, Peebles CL, Gegenheimer P, Abelson J, (1983) Mechanism of action of a yeast RNA ligase in tRNA splicing. Cell 32: 537-546
26. Popow J, Englert M, Weitzer S, Schleiffer A, Mierzwa B, Mechtler K, Trowitzsch S, Will CL, Lührmann R, Söll D, et al, (2011) HSPC117 is the essential subunit of a human tRNA splicing ligase complex. Science 331: 760-764
27. Ali MMU, Bagratuni T, Davenport EL, Nowak PR, Silva-Santisteban MC, Hardcastle A, McAndrews C, Rowlands MG, Morgan GJ, Aherne W, et al, (2011) Structure of the Ire1 autophosphorylation complex and implications for the unfolded protein response. EMBO J 30: 894-905
28. Lee KPK, Dey M, Neculai D, Cao C, Dever TE, Sicheri F, (2008) Structure of the dual enzyme Ire1 reveals the basis for catalysis and regulation in nonconventional RNA splicing. Cell 132: 89-100
29. Aragón T, van Anken E, Pincus D, Serafimova IM, Korennykh AV, Rubio CA, Walter P, (2009) Messenger RNA targeting to endoplasmic reticulum stress signalling sites. Nature 457: 736-740
30. Li H, Korennykh AV, Behrman SL, Walter P, (2010) Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering. Proc Natl Acad Sci USA 107: 16113-16118
31. Joshi A, Newbatt Y, McAndrew PC, Stubbs M, Burke R, Richards MW, Bhatia C, Caldwell JJ, McHardy T, Collins I, et al, (2015) Molecular mechanisms of human IRE1 activation through dimerization and ligand binding. Oncotarget 6: 13019-13035
32. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410
33. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al, (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948
34. Zuker M, (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415
35. Popenda M, Szachniuk M, Antczak M, Purzycka KJ, Lukasiak P, Bartol N, Blazewicz J, Adamiak RW, (2012) Automated 3D structure composition for large RNAs. Nucleic Acids Res 40: e112-e112
36. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D, (2002) The human genome browser at UCSC. Genome Res 12: 996-1006
37. Mendez AS, Alfaro J, Morales-Soto MA, Dar AC, McCullagh E, Gotthardt K, Li H, Acosta-Alvear D, Sidrauski C, Korennykh AV, et al, (2015) Endoplasmic reticulum stress-independent activation of unfolded protein response kinases by a small molecule ATP-mimic. eLife 4: e05434
38. Popow J, Jurkin J, Schleiffer A, Martinez J, (2014) Analysis of orthologous groups reveals archease and DDX1 as tRNA splicing factors. Nature 511: 104-107
39. Iwawaki T, Akai R, Kohno K, Miura M, (2004) A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat Med 10: 98-102