Peptides derived from the bifunctional kinase/RNase enzyme IRE1α modulate IRE1α activity and protect cells from endoplasmic reticulum stress

FASEB Journal

Volumn 25, Issue 9, 2011, Pages 3115-3129

  Bouchecareilh, Marion ^a,b   Higa, Arisa ^a   Fribourg, Sébastien ^a,c   Moenner, Michel ^a,b   Chevet, Eric ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSERM   (France)

^c INSTITUT EUROPÉEN DE CHIMIE ET BIOLOGIE   (France)

Author keywords

Alphascreen; RIDD; UPR

Indexed keywords

COMPLEMENTARY DNA; PHOSPHOTRANSFERASE; PROTEIN IRE1; RIBONUCLEASE; STRESS ACTIVATED PROTEIN KINASE; TUNICAMYCIN; X BOX BINDING PROTEIN 1;

APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CATALYSIS; CELL CULTURE; CELL PROTECTION; CELL SURVIVAL; CELLULAR STRESS SIGNAL; CROSS LINKING; CYTOTOXICITY; DNA TRANSFECTION; ENDOPLASMIC RETICULUM STRESS; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; RNA CLEAVAGE; RNA SPLICING; UNFOLDED PROTEIN RESPONSE;

ANIMALS; CAENORHABDITIS ELEGANS; CELL LINE, TUMOR; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; GENE EXPRESSION REGULATION; HUMANS; MAP KINASE KINASE 4; MODELS, MOLECULAR; PEPTIDES; PROTEIN CONFORMATION; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

CAENORHABDITIS ELEGANS;

EID: 80052668828     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-182931     Document Type: Article

References (34)

1. Schroder, M., and Kaufman, R. J. (2005) The mammalian unfolded protein response. Annu. Rev. Biochem. 74, 739-789 (Pubitemid 40995523)
2. Harding, H. P., Zhang, Y., and Ron, D. (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274 (Pubitemid 29051178)
3. Novoa, I., Zeng, H., Harding, H. P., and Ron, D. (2001) Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J. Cell Biol. 153, 1011-1022
4. Nadanaka, S., Okada, T., Yoshida, H., and Mori, K. (2007) Role of disulfide bridges formed in the luminal domain of ATF6 in sensing endoplasmic reticulum stress. Mol. Cell. Biol. 27, 1027-1043 (Pubitemid 46174565)
5. Haze, K., Yoshida, H., Yanagi, H., Yura, T., and 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 (Pubitemid 29534025)
6. Ron, D., and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell. Biol. 8, 519-529 (Pubitemid 46985379)
7. Credle, J. J., Finer-Moore, J. S., Papa, F. R., Stroud, R. M., and Walter, P. (2005) On the mechanism of sensing unfolded protein in the endoplasmic reticulum. Proc. Natl. Acad. Sci. U. S. A. 102, 18773-18784 (Pubitemid 43049523)
8. Lee, K. P., Dey, M., Neculai, D., Cao, C., Dever, T. E., and Sicheri, F. (2008) Structure of the dual enzyme Ire1 reveals the basis for catalysis and regulation in nonconventional RNA splicing. Cell 132, 89-100
9. Korennykh, A. V., Egea, P. F., Korostelev, A. A., Finer-Moore, J., Zhang, C., Shokat, K. M., Stroud, R. M., and Walter, P. (2009) The unfolded protein response signals through high-order assembly of Ire1. Nature 457, 687-693
10. Aragon, T., Van Anken, E., Pincus, D., Serafimova, I. M., Korennykh, A. V., Rubio, C. A., and Walter, P. (2009) Messenger RNA targeting to endoplasmic reticulum stress signalling sites. Nature 457, 736-740
11. Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., Harding, H. P., and Ron, D. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666 (Pubitemid 30070916)
12. Nguyen, D. T., Kebache, S., Fazel, A., Wong, H. N., Jenna, S., Emadali, A., Lee, E. H., Bergeron, J. J., Kaufman, R. J., Larose, L., and Chevet, E. (2004) Nck-dependent activation of extracellular signal-regulated kinase-1 and regulation of cell survival during endoplasmic reticulum stress. Mol. Biol. Cell 15, 4248-4260 (Pubitemid 39122027)
13. Moenner, M., Pluquet, O., Bouchecareilh, M., and Chevet, E. (2007) Integrated endoplasmic reticulum stress responses in cancer. Cancer Res. 67, 10631-10634 (Pubitemid 350145884)
14. Han, D., Lerner, A. G., Vande Walle, L., Upton, J. P., Xu, W., Hagen, A., Backes, B. J., Oakes, S. A., and Papa, F. R. (2009) IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138, 562-575
15. Lin, J. H., Li, H., Yasumura, D., Cohen, H. R., Zhang, C., Panning, B., Shokat, K. M., Lavail, M. M., and Walter, P. (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318, 944-949 (Pubitemid 350098984)
16. Wiseman, R. L., Zhang, Y., Lee, K. P., Harding, H. P., Haynes, C. M., Price, J., Sicheri, F., and Ron, D. (2010) Flavonol activation defines an unanticipated ligand-binding site in the kinase-RNase domain of IRE1. Mol. Cell 38, 291-304
17. Papandreou, I., Denko, N. C., Olson, M., Van Melckebeke, H., Lust, S., Tam, A., Solow-Cordero, D. E., Bouley, D. M., Offner, F., Niwa, M., and Koong, A. C. (2010) Identification of an Ire1alpha endonuclease specific inhibitor with cytotoxic activity against human multiple myeloma. Blood 117, 1311-1314
18. Volkmann, K., Lucas, J. L., Vuga, D., Wang, X., Brumm, D., Stiles, C., Kriebel, D., Der-Sarkissian, A., Krishnan, K., Schweitzer, C., Liu, Z., Malyankar, U. M., Chiovitti, D., Canny, M., Durocher, D., Sicheri, F., and Patterson, J. B. (2011) Potent and selective inhibitors of the inositol-requiring enzyme 1 endoribonuclease. J. Biol. Chem. 286, 12743-12755
19. Lee, K. P., and Sicheri, F. (2011) Principles of IRE1 modulation using chemical tools. Methods Enzymol. 490, 271-294
20. Hollien, J., Lin, J. H., Li, H., Stevens, N., Walter, P., and Weissman, J. S. (2009) Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 186, 323-331
21. Schwarze, S. R., Ho, A., Vocero-Akbani, A., and Dowdy, S. F. (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285, 1569-1572 (Pubitemid 29420581)
22. Bouchecareilh, M., Caruso, M. E., Roby, P., Parent, S., Rouleau, N., Taouji, S., Pluquet, O., Bosse, R., Moenner, M., and Chevet, E. (2010) AlphaScreen-based characterization of the bifunctional kinase/RNase IRE1alpha: a novel and atypical drug target. J. Biomol. Screen. 15, 406-417
23. Jenna, S., Caruso, M. E., Emadali, A., Nguyen, D. T., Dominguez, M., Li, S., Roy, R., Reboul, J., Vidal, M., Tzimas, G. N., Bosse, R., and Chevet, E. (2005) Regulation of membrane trafficking by a novel Cdc42-related protein in Caenorhabditis elegans epithelial cells. Mol. Biol. Cell 16, 1629-1639 (Pubitemid 40471936)
24. Delom, F., Fessart, D., Caruso, M. E., and Chevet, E. (2007) Tat-mediated protein delivery in living Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 352, 587-591 (Pubitemid 44895453)
25. Caruso, M. E., Jenna, S., Bouchecareilh, M., Baillie, D. L., Boismenu, D., Halawani, D., Latterich, M., and Chevet, E. (2008) GTPase-mediated regulation of the unfolded protein response in Caenorhabditis elegans is dependent on the AAA+ ATPase CDC-48. Mol. Cell. Biol. 28, 4261-4274 (Pubitemid 351904949)
26. Drogat, B., Auguste, P., Nguyen, D. T., Bouchecareilh, M., Pineau, R., Nalbantoglu, J., Kaufman, R. J., Chevet, E., Bikfalvi, A., and Moenner, M. (2007) IRE1 signaling is essential for ischemia-induced vascular endothelial growth factor-A expression and contributes to angiogenesis and tumor growth in vivo. Cancer Res. 67, 6700-6707 (Pubitemid 47105516)
27. Finney, M., and Ruvkun, G. (1990) The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63, 895-905 (Pubitemid 120034931)
28. Kanemoto, S., Kondo, S., Ogata, M., Murakami, T., Urano, F., and Imaizumi, K. (2005) XBP1 activates the transcription of its target genes via an ACGT core sequence under ER stress. Biochem. Biophys. Res. Commun. 331, 1146-1153 (Pubitemid 40692478)
29. Hollien, J., and Weissman, J. S. (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313, 104-107 (Pubitemid 44051264)
30. Borsello, T., Clarke, P. G., Hirt, L., Vercelli, A., Repici, M., Schorderet, D. F., Bogousslavsky, J., and Bonny, C. (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat. Med. 9, 1180-1186 (Pubitemid 37173703)
31. Lee, K., Tirasophon, W., Shen, X., Michalak, M., Prywes, R., Okada, T., Yoshida, H., Mori, K., and Kaufman, R. J. (2002) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16, 452-466 (Pubitemid 34165102)
32. Shen, X., Ellis, R. E., Sakaki, K., and Kaufman, R. J. (2005) Genetic interactions due to constitutive and inducible gene regulation mediated by the unfolded protein response in C. elegans. PLoS Genet. 1, e37
33. Urano, F., Calfon, M., Yoneda, T., Yun, C., Kiraly, M., Clark, S. G., and Ron, D. (2002) A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. J. Cell Biol. 158, 639-646 (Pubitemid 34920103)
34. Papa, F. R., Zhang, C., Shokat, K., and Walter, P. (2003) Bypassing a kinase activity with an ATP-competitive drug. Science 302, 1533-1537 (Pubitemid 37475689)