IRE1α-dependent decay of CReP/Ppp1r15b mRNA increases eukaryotic initiation factor 2α phosphorylation and suppresses protein synthesis

Molecular and Cellular Biology

Volumn 35, Issue 16, 2015, Pages 2761-2770

  So, Jae Seon ^a   Cho, Sungyun ^a   Min, Sang Hyun ^b   Kimball, Scot R ^c   Lee, Ann Hwee ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Daegu Gyeongbuk Medical Innovation Foundation   (South Korea)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CREP PROTEIN; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PHOSPHATASE; PROTEIN IRE1; PROTEIN IRE1 ALPHA; REGULATOR PROTEIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; DNA BINDING PROTEIN; ERN1 PROTEIN, MOUSE; INITIATION FACTOR 2; PHOSPHOPROTEIN PHOSPHATASE 1; PPP1R15B PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE; REGULATORY FACTOR X TRANSCRIPTION FACTORS; RIBONUCLEASE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRESS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; ENZYME SUBUNIT; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; LIVER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; TRANSLATION REGULATION; UNFOLDED PROTEIN RESPONSE; ANIMAL; C57BL MOUSE; CHEMISTRY; DOWN REGULATION; GENE INACTIVATION; GENETICS; METABOLISM; PHOSPHORYLATION; RNA STABILITY;

EUKARYOTA; MUS;

ANIMALS; DNA-BINDING PROTEINS; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; EUKARYOTIC INITIATION FACTOR-2; GENE KNOCKOUT TECHNIQUES; LIVER; MICE, INBRED C57BL; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN PHOSPHATASE 1; PROTEIN-SERINE-THREONINE KINASES; RNA STABILITY; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 84937841076     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00215-15     Document Type: Article

References (43)

1. Walter P, Ron D. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-1086. http://dx.doi .org/10.1126/science.1209038
2. Hetz C, Martinon F, Rodriguez D, Glimcher LH. 2011. The unfolded protein response: integrating stress signals through the stress sensor IRE1_. Physiological Rev 91:1219-1243. http://dx.doi.org/10.1152/physrev.00001.2011
3. Ron D, Walter P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519-529. http://dx .doi.org/10.1038/nrm2199
4. Schroder M, Kaufman RJ. 2005. The mammalian unfolded protein response. Annu Rev Biochem 74:739-789. http://dx.doi.org/10.1146/annurev .biochem.73.011303.074134
5. Gardner BM, Pincus D, Gotthardt K, Gallagher CM, Walter P. 2013. Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol 5:a013169. http://dx.doi.org/10.1101/cshperspect .a013169
6. 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. http://dx.doi.org/10.1016/j.molcel.2007.06.011
7. Lee A-H, Iwakoshi NN, Glimcher LH. 2003. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23:7448-7459. http://dx.doi.org/10.1128/MCB .23.21.7448-7459.2003
8. Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, Lee AH, Qian SB, Zhao H, Yu X, Yang L, Tan BK, Rosenwald A, Hurt EM, Petroulakis E, Sonenberg N, Yewdell JW, Calame K, Glimcher LH, Staudt LM. 2004. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21:81-93. http://dx.doi.org/10.1016/j.immuni.2004.06.010
9. 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. http://dx.doi.org/10.1083/jcb.200903014
10. Oikawa D, Tokuda M, Hosoda A, Iwawaki T. 2010. Identification of a consensus element recognized and cleaved by IRE1_. Nucleic Acids Res 38:6265-6273. http://dx.doi.org/10.1093/nar/gkq452
11. Han D, Lerner AG, Vande Walle L, Upton J-P, Xu W, Hagen A, Backes BJ, Oakes SA, Papa FR. 2009. IRE1_ kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138:562-575. http://dx.doi.org/10.1016/j.cell.2009.07.017
12. Hollien J, Weissman JS. 2006. Decay of endoplasmic reticulum-localized mRNAsduring the unfolded protein response. Science 313:104-107. http://dx.doi.org/10.1126/science.1129631
13. So J-S, Hur Kyu Y, Tarrio M, Ruda V, Frank-Kamenetsky M, Fitzgerald K, Koteliansky V, Lichtman Andrew H, Iwawaki T, Glimcher Laurie H, Lee A-H. 2012. Silencing of lipid metabolism genes through IRE1_- mediated mRNA decay lowers plasma lipids in mice. Cell Metab 16:487-499. http://dx.doi.org/10.1016/j.cmet.2012.09.004
14. Hur KY, So J-S, Ruda V, Frank-Kamenetsky M, Fitzgerald K, Koteliansky V, Iwawaki T, Glimcher LH, Lee A-H. 2012. IRE1_ activation protects mice against acetaminophen-induced hepatotoxicity. J Exp Med 209:307-318. http://dx.doi.org/10.1084/jem.20111298
15. Binet F, Mawambo G, Sitaras N, Tetreault N, Lapalme E, Favret S, Cerani A, Leboeuf D, Tremblay S, Rezende F, Juan AM, Stahl A, Joyal JS, Milot E, Kaufman RJ, Guimond M, Kennedy TE, Sapieha P. 2013. Neuronal ER stress impedes myeloid-cell-induced vascular regeneration through IRE1_ degradation of netrin-1. Cell Metab 17:353-371. http://dx .doi.org/10.1016/j.cmet.2013.02.003
16. Osorio F, Tavernier SJ, Hoffmann E, Saeys Y, Martens L, Vetters J, Delrue I, De Rycke R, Parthoens E, Pouliot P, Iwawaki T, Janssens S, Lambrecht BN. 2014. The unfolded-protein-response sensor IRE-1_ regulates the function of CD8__ dendritic cells. Nat Immunol 15:248-257. http://dx.doi.org/10.1038/ni.2808
17. Lee AH, Heidtman K, Hotamisligil GS, Glimcher LH. 2011. Dual and opposing roles of the unfolded protein response regulated by IRE1_ and XBP1 in proinsulin processing and insulin secretion. Proc Natl Acad Sci U S A 108:8885-8890. http://dx.doi.org/10.1073/pnas.1105564108
18. Harding HP, Zhang Y, Ron D. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274. http://dx.doi.org/10.1038/16729
19. Mori K. 2000. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101:451-454. http://dx.doi.org/10.1016/S0092-8674(00)80855-7
20. Ron D Harding HP. 2012. Protein-folding homeostasis in the endoplasmic reticulum and nutritional regulation. Cold Spring Harb Perspect Biol 4:a013177. http://dx.doi.org/10.1101/cshperspect.a013177
21. Hinnebusch AG. 2000. Mechanism and regulation of initiator methionyltRNA binding to ribosomes in translational control of gene expression. Cold Spring Harbor Monogr Arch 2000:503-527.
22. Pavitt GD, Ron D. 2012. New insights into translational regulation in the endoplasmic reticulum unfolded protein response. Cold Spring Harb Perspect Biol 4:a012278. http://dx.doi.org/10.1101/cshperspect.a012278
23. Novoa I, Zeng H, Harding HP, Ron D. 2001. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2_. J Cell Biol 153:1011-1022. http://dx.doi.org/10.1083/jcb.153.5.1011
24. Jousse Cl., Oyadomari S, Novoa I, Lu P, Zhang Y, Harding HP, Ron D. 2003. Inhibition of a constitutive translation initiation factor 2_ phosphatase, CReP, promotes survival of stressed cells. J Cell Biol 163:767-775. http://dx.doi.org/10.1083/jcb.200308075
25. Ma Y, Hendershot LM. 2003. Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J Biol Chem 278:34864-34873. http://dx.doi.org/10.1074/jbc.M301107200
26. Lee A-H, Scapa EF, Cohen DE, Glimcher LH. 2008. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320:1492-1496. http://dx.doi.org/10.1126/science.1158042
27. Iwawaki T, Akai R, Yamanaka S, Kohno K. 2009. Function of IRE1_ in the placenta is essential for placental development and embryonic viability. Proc Natl Acad Sci USA 106:16657-16662. http://dx.doi.org/10.1073/pnas.0903775106
28. Hetz C, Bernasconi P, Fisher J, Lee AH, Bassik MC, Antonsson B, Brandt GS, Iwakoshi NN, Schinzel A, Glimcher LH, Korsmeyer SJ. 2006. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1_. Science 312:572-576. http://dx .doi.org/10.1126/science.1123480
29. Kimball SR, Everson WV, Flaim KE, Jefferson LS. 1989. Initiation of protein synthesis in a cell-free system prepared from rat hepatocytes. Am J Physiol Cell Physiol 256:C28-C34.
30. Tirasophon W, Welihinda AA, Kaufman RJ. 1998. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev 12:1812-1824. http://dx.doi.org/10.1101/gad.12.12.1812
31. Baird TD, Wek RC. 2012. Eukaryotic initiation factor 2 phosphorylation and translational control in metabolism. Adv Nutr 3:307-321. http://dx .doi.org/10.3945/an.112.002113
32. Maurel M, Chevet E, Tavernier J, Gerlo S. 2014. Getting RIDD of RNA:IRE1 in cell fate regulation. Trends Biochem Sci 39:245-254. http://dx.doi .org/10.1016/j.tibs.2014.02.008
33. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099-1108. http://dx.doi.org/10.1016/S1097-2765(00)00108-8
34. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S, Kaufman RJ. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7:1165-1176. http://dx.doi.org/10.1016/S1097-2765(01)00265-9
35. Dey S, Baird TD, Zhou D, Palam LR, Spandau DF, Wek RC. 2010. Both transcriptional regulation and translational control of ATF4 are central to the integrated stress response. J Biol Chem 285:33165-33174. http://dx .doi.org/10.1074/jbc.M110.167213
36. Jiang HY, Wek RC. 2005. GCN2 phosphorylation of eIF2_ activates NF-_B in response to UV irradiation. Biochem J 385:371-380. http://dx .doi.org/10.1042/BJ20041164
37. Harding HP, Zhang Y, Scheuner D, Chen J-J, Kaufman RJ, Ron D. 2009. Ppp1r15 gene knockout reveals an essential role for translation initiation factor 2_ (eIF2_) dephosphorylation in mammalian development. Proc Natl Acad Sci USA 106:1832-1837. http://dx.doi.org/10.1073/pnas .0809632106
38. Harding HP, Zeng H, Zhang Y, Jungries R, Chung P, Plesken H, Sabatini DD, Ron D. 2001. Diabetes mellitus and exocrine pancreatic dysfunction in Perk/ mice reveals a role for translational control in secretory cell survival. Mol Cell 7:1153-1163. http://dx.doi.org/10.1016 /S1097-2765(01)00264-7
39. Zhang P, McGrath B, Li S, Frank A, Zambito F, Reinert J, Gannon M, Ma K, McNaughton K, Cavener DR. 2002. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol Cell Biol 22:3864-3874. http://dx.doi.org/10.1128/MCB.22.11.3864-3874.2002
40. Wei J, Sheng X, Feng D, McGrath B, Cavener DR. 2008. PERK is essential for neonatal skeletal development to regulate osteoblast proliferation and differentiation. J Cell Physiol 217:693-707. http://dx.doi.org/10.1002/jcp.21543
41. Zhang W, Feng D, Li Y, Iida K, McGrath B, Cavener DR. 2006. PERK EIF2AK3 control of pancreatic beta cell differentiation and proliferation is required for postnatal glucose homeostasis. Cell Metab 4:491-497. http://dx.doi.org/10.1016/j.cmet.2006.11.002
42. Boyce M, Bryant KF, Jousse Cl Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J. 2005. A selective inhibitor of eIF2_ dephosphorylation protects cells from ER stress. Science 307:935-939. http://dx.doi.org/10.1126/science.1101902
43. Tsaytler P, Harding HP, Ron D, Bertolotti A. 2011. Selective inhibition of a regulatory subunit of protein phosphatase 1 restores proteostasis. Science 332:91-94. http://dx.doi.org/10.1126/science.1201396