Cotranslational Targeting of XBP1 Protein to the Membrane Promotes Cytoplasmic Splicing of Its Own mRNA

Molecular Cell

Volumn 34, Issue 2, 2009, Pages 191-200

  Yanagitani, Kota ^a   Imagawa, Yusuke ^a   Iwawaki, Takao ^b   Hosoda, Akira ^b   Saito, Michiko ^a   Kimata, Yukio ^a   Kohno, Kenji ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b RIKEN   (Japan)

Author keywords

PROTEINS; RNA; SIGNALING

Indexed keywords

MESSENGER RNA; PROTEIN IRE1; PUROMYCIN; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL MEMBRANE; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; CYTOSOL; ENDOPLASMIC RETICULUM; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYDROPHOBICITY; MOUSE; NONHUMAN; PROTEIN LOCALIZATION; RNA SPLICING; RNA TRANSLATION;

ANIMALS; BASE SEQUENCE; CYTOPLASM; DNA-BINDING PROTEINS; ENDORIBONUCLEASES; HUMANS; INTRACELLULAR MEMBRANES; MICE; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RIBOSOMES; RNA SPLICING; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 64749103329     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.02.033     Document Type: Article

References (36)

1. Aragón T., van Anken E., Pincus D., Serafimova I.M., Korennykh A.V., Rubio C.A., and Walter P. Messenger RNA targeting to endoplasmic reticulum stress signaling sites. Nature 457 (2009) 736-740
2. Back S.H., Lee K., Vink E., and Kaufman R.J. Cytoplasmic IRE1alpha-mediated XBP1 mRNA splicing in the absence of nuclear processing and endoplasmic reticulum stress. J. Biol. Chem. 281 (2006) 18691-18706
3. Calfon M., Zeng H., Urano F., Till J.H., Hubbard S.R., Harding H.P., Clark S.G., and Ron D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415 (2002) 92-96
4. Cox J.S., and Walter P. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87 (1996) 391-404
5. Cox J.S., Shamu C.E., and Walter P. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73 (1993) 1197-1206
6. Diehn M., Eisen M.B., Botstein D., and Brown P.O. Large-scale identification of secreted and membrane-associated gene products using DNA microarrays. Nat. Genet. 25 (2000) 58-62
7. Du T.G., Schmid M., and Jansen R.P. Why cells move messages: the biological functions of mRNA localization. Semin. Cell Dev. Biol. 18 (2007) 171-177
8. Hollien J., and Weissman J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313 (2006) 104-107
9. Imagawa Y., Hosoda A., Sasaka S., Tsuru A., and Kohno K. RNase domains determine the functional difference between IRE1alpha and IRE1beta. FEBS Lett. 582 (2008) 656-660
10. Iwawaki T., and Akai R. Analysis of the XBP1splicing mechanism using endoplasmic reticulum stress-indicators. Biochem. Biophys. Res. Commun. 350 (2006) 709-715
11. Iwawaki T., Hosoda A., Okuda T., Kamigori Y., Nomura-Furuwatari C., Kimata Y., Tsuru A., and Kohno K. Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat. Cell Biol. 3 (2001) 158-164
12. Kimata Y., Ishiwata-Kimata Y., Yamada S., and Kohno K. Yeast unfolded protein response pathway regulates expression of genes for anti-oxidative stress and for cell surface proteins. Genes Cells 11 (2006) 59-69
13. Kimata Y., Ishiwata-Kimata Y., Ito T., Hirata A., Suzuki T., Oikawa D., Takeuchi M., and Kohno K. Two regulatory steps of ER-stress sensor Ire1 involving its cluster formation and interaction with unfolded proteins. J. Cell Biol. 179 (2007) 75-86
14. Kohno K., Normington K., Sambrook J., Gething M.J., and Mori K. The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol. Cell. Biol. 13 (1993) 877-890
15. Kowarik M., Kung S., Martoglio B., and Helenius A. Protein folding during cotranslational translocation in the endoplasmic reticulum. Mol. Cell 10 (2002) 769-778
16. Mathews D.H., Sabina J., Zuker M., and Turner D.H. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288 (1999) 911-940
17. Mori K., Sant A., Kohno K., Normington K., Gething M.J., and Sambrook J.F. A 22 bp cis-acting element is necessary and sufficient for the induction of the yeast KAR2 (BiP) gene by unfolded proteins. EMBO J. 11 (1992) 2583-2593
18. Mori K., Ma W., Gething M.J., and Sambrook J. A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74 (1993) 743-756
19. Mori K., Kawahara T., Yoshida H., Yanagi H., and Yura T. Signalling from endoplasmic reticulum to nucleus: transcription factor with a basic-leucine zipper motif is required for the unfolded protein-response pathway. Genes Cells 1 (1996) 803-817
20. Palacios I.M., and St Johnston D. Getting the message across: the intracellular localization of mRNAs in higher eukaryotes. Annu. Rev. Cell Dev. Biol. 17 (2001) 569-614
21. Ron D., and Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8 (2007) 519-529
22. Rüegsegger U., Leber J.H., and Walter P. Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107 (2001) 103-114
23. Shamu C.E., and Walter P. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J. 15 (1996) 3028-3039
24. Shen X., Ellis R.E., Lee K., Liu C.Y., Yang K., Solomon A., Yoshida H., Morimoto R., Kurnit D.M., Mori K., and Kaufman R.J. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107 (2001) 893-903
25. Sidrauski C., and Walter P. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90 (1997) 1031-1039
26. Stephens S.B., Dodd R.D., Brewer J.W., Lager P.J., Keene J.D., and Nicchitta C.V. Stable ribosome binding to the endoplasmic reticulum enables compartment-specific regulation of mRNA translation. Mol. Biol. Cell 16 (2005) 5819-5831
27. Tirasophon W., Welihinda A.A., and Kaufman R.J. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev. 12 (1998) 1812-1824
28. Travers K.J., Patil C.K., Wodicka L., Lockhart D.J., Weissman J.S., and Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101 (2000) 249-258
29. Wang X.Z., Harding H.P., Zhang Y., Jolicoeur E.M., Kuroda M., and Ron D. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J. 17 (1998) 5708-5717
30. Welihinda A.A., and Kaufman R.J. The unfolded protein response pathway in Saccharomyces cerevisiae. Oligomerization and trans-phosphorylation of Ire1p (Ern1p) are required for kinase activation. J. Biol. Chem. 271 (1996) 18181-18187
31. Wu J., Rutkowski D.T., Dubois M., Swathirajan J., Saunders T., Wang J., Song B., Yau G.D., and Kaufman R.J. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev. Cell 13 (2007) 351-364
32. Yamamoto K., Sato T., Matsui T., Sato M., Okada T., Yoshida H., Harada A., and Mori K. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev. Cell 13 (2007) 365-376
33. Yoshida H., Matsui T., Yamamoto A., Okada T., and Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107 (2001) 881-891
34. Yoshida H., Matsui T., Hosokawa N., Kaufman R.J., Nagata K., and Mori K. A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell 4 (2003) 265-271
35. Yoshida H., Oku M., Suzuki M., and Mori K. pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J. Cell Biol. 172 (2006) 565-575
36. Yoshihisa T., Ohshima C., Yunoki-Esaki K., and Endo T. Cytoplasmic splicing of tRNA in Saccharomyces cerevisiae. Genes Cells 12 (2007) 285-297