ATF6α Optimizes Long-Term Endoplasmic Reticulum Function to Protect Cells from Chronic Stress

Developmental Cell

Volumn 13, Issue 3, 2007, Pages 351-364

  Wu, Jun ^a   Rutkowski, D Thomas ^a   Dubois, Meghan ^a   Swathirajan, Jayanth ^a   Saunders, Thomas ^a   Wang, Junying ^a   Song, Benbo ^a   Yau, Grace D Y ^a   Kaufman, Randal J ^a,b  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

PROTEINS; SIGNALING

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ACTIVATING TRANSCRIPTION FACTOR 6ALPHA; CHAPERONE; MEMBRANE PROTEIN; PROTEIN IRE1; PROTEIN IRE1ALPHA; PROTEIN PERK; UNCLASSIFIED DRUG; ATF6ALPHA PROTEIN, MOUSE; CRE RECOMBINASE; DITHIOERYTHRITOL; INTEGRASE; MESSENGER RNA; THIOL REAGENT; TRANSACTIVATOR PROTEIN; TUNICAMYCIN;

ARTICLE; CELL FUNCTION; CELL NUCLEUS; CELL PROTECTION; CELL STRESS; CELL SURVIVAL; CHRONIC STRESS; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENDOPLASMIC RETICULUM; FEMALE; GENE CONTROL; GENE DELETION; GENE TARGETING; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN SECRETION; SIGNAL TRANSDUCTION; VERTEBRATE; ALLELE; ANIMAL; C57BL MOUSE; CELL CULTURE; CHRONIC DISEASE; CROSS BREEDING; EXON; FIBROBLAST; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MOUSE MUTANT; OXIDATIVE STRESS; TRANSGENIC MOUSE;

ANIMALIA; VERTEBRATA;

ACTIVATING TRANSCRIPTION FACTOR 6; ALLELES; ANIMALS; CELLS, CULTURED; CHRONIC DISEASE; CROSSES, GENETIC; DITHIOERYTHRITOL; ENDOPLASMIC RETICULUM; EXONS; FIBROBLASTS; GENE DELETION; GENE EXPRESSION PROFILING; INTEGRASES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OXIDATIVE STRESS; PROTEIN FOLDING; RNA, MESSENGER; SULFHYDRYL REAGENTS; TRANS-ACTIVATORS; TUNICAMYCIN;

EID: 34548189283     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2007.07.005     Document Type: Article

References (52)

1. Baumeister P., Luo S., Skarnes W.C., Sui G., Seto E., Shi Y., and Lee A.S. Endoplasmic reticulum stress induction of the Grp78/BiP promoter: Activating mechanisms mediated by YY1 and its interactive chromatin modifiers. Mol. Cell. Biol. 25 (2005) 4529-4540
2. 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
3. Carrasco D.R., Sukhdeo K., Protopopova M., Sinha R., Enos M., Carrasco D.E., Zheng M., Mani M., Henderson J., Pinkus G.S., et al. The differentiation and stress response factor XBP-1 drives multiple myeloma pathogenesis. Cancer Cell 11 (2007) 349-360
4. Fawcett T.W., Martindale J.L., Guyton K.Z., Hai T., and Holbrook N.J. Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem. J. 339 (1999) 135-141
5. Gal-Yam E.N., Jeong S., Tanay A., Egger G., Lee A.S., and Jones P.A. Constitutive nucleosome depletion and ordered factor assembly at the GRP78 promoter revealed by single molecule footprinting. PLoS Gen. 2 (2006) e160 10.1371/journal.pgen.0020160
6. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., Ellis B., Gautier L., Ge Y., Gentry J., et al. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol. 5 (2004) R80
7. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., and Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6 (2000) 1099-1108
8. Harding H.P., Zhang Y., Bertolotti A., Zeng H., and Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5 (2000) 897-904
9. Harding H.P., Zhang Y., and Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397 (1999) 271-274
10. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., Sadri N., Yun C., Popko B., Paules R., et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11 (2003) 619-633
11. Haze K., Okada T., Yoshida H., Yanagi H., Yura T., Negishi M., and Mori K. Identificaiton of the G13 (cAMP-response-element-binding protein-related protein) gene product related to activating transcription factor 6 as a transcriptional activator of the mammalian unfolded protein response. Biochem. J. 355 (2001) 19-28
12. Haze K., Yoshida H., Yanagi H., Yura T., and Mori K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10 (1999) 3787-3799
13. Hendershot L.M. The ER chaperone BiP is a master regulator of ER function. Mt. Sinai J. Med. 71 (2004) 289-297
14. Hetz C., Bernasconi P., Fisher J., Lee A.H., Bassik M.C., Antonsson B., Brandt G.S., Iwakoshi N.N., Schinzel A., Glimcher L.H., et al. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 312 (2006) 572-576
15. Hiraoka M., Abe A., Lu Y., Yang K., Han X., Gross R.W., and Shayman J.A. Lysosomal phospholipase A2 and phospholipidosis. Mol. Cell. Biol. 26 (2006) 6139-6148
16. Hollien J., and Weissman J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313 (2006) 104-107
17. Hong M., Luo S., Baumeister P., Huang J.M., Gogia R.K., Li M., and Lee A.S. Underglycosylation of ATF6 as a novel sensing mechanism for activation of the unfolded protein response. J. Biol. Chem. 279 (2004) 11354-11363
18. Hung C.C., Ichimura T., Stevens J.L., and Bonventre J.V. Protection of renal epithelial cells against oxidative injury by endoplasmic reticulum stress preconditioning is mediated by ERK1/2 activation. J. Biol. Chem. 278 (2003) 29317-29326
19. Kang S.W., Rane N.S., Kim S.J., Garrison J.L., Taunton J., and Hegde R.S. Substrate-Specific Translocational Attenuation during ER Stress Defines a Pre-Emptive Quality Control Pathway. Cell 127 (2006) 999-1013
20. Lee A.H., Iwakoshi N.N., and Glimcher L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23 (2003) 7448-7459
21. Lee K., Tirasophon W., Shen X., Michalak M., Prywes R., Okada T., Yoshida H., Mori K., and Kaufman R.J. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16 (2002) 452-466
22. Li M., Baumeister P., Roy B., Phan T., Foti D., Luo S., and Lee A.S. ATF6 as a transcription activator of the endoplasmic reticulum stress element: Thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1. Mol. Cell. Biol. 20 (2000) 5096-5106
23. Lu P.D., Harding H.P., and Ron D. Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol. 167 (2004) 27-33
24. Lu P.D., Jousse C., Marciniak S.J., Zhang Y., Novoa I., Scheuner D., Kaufman R.J., Ron D., and Harding H.P. Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J. 23 (2004) 169-179
25. Luo S., Baumeister P., Yang S., Abcouwer S.F., and Lee A.S. Induction of Grp78/BiP by translational block: Activation of the Grp78 promoter by ATF4 through and upstream ATF/CRE site independent of the endoplasmic reticulum stress elements. J. Biol. Chem. 278 (2003) 37375-37385
26. Ma Y., Brewer J.W., Diehl J.A., and Hendershot L.M. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318 (2002) 1351-1365
27. Marciniak S.J., and Ron D. Endoplasmic reticulum stress signaling in disease. Physiol. Rev. 86 (2006) 1133-1149
28. Marciniak S.J., Yun C.Y., Oyadomari S., Novoa I., Zhang Y., Jungreis R., Nagata K., Harding H.P., and Ron D. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18 (2004) 3066-3077
29. Nadanaka S., Yoshida H., and Mori K. Reduction of disulfide bridges in the lumenal domain of ATF6 in response to glucose starvation. Cell Struct. Funct. 31 (2006) 127-134
30. Novoa I., Zhang Y., Zeng H., Jungreis R., Harding H.P., and Ron D. Stress-induced gene expression requires programmed recovery from translational repression. EMBO J. 22 (2003) 1180-1187
31. Okada T., Haze K., Nadanaka S., Yoshida H., Seidah N.G., Hirano Y., Sato R., Negishi M., and Mori K. A serine protease inhibitor prevents endoplasmic reticulum stress-induced cleavage but not transport of the membrane-bound transcription factor ATF6. J. Biol. Chem. 278 (2003) 31024-31032
32. Okada T., Yoshida H., Akazawa R., Negishi M., and Mori K. Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem. J. 366 (2002) 585-594
33. Reimold A.M., Iwakoshi N.N., Manis J., Vallabhajosyula P., Szomolanyi-Tsuda E., Gravallese E.M., Friend D., Grusby M.J., Alt F., and Glimcher L.H. Plasma cell differentiation requires the transcription factor XBP-1. Nature 412 (2001) 300-307
34. Rutkowski D.T., Arnold S.M., Miller C.N., Wu J., Li J., Gunnison K.M., Mori K., Sadighi Akha A.A., Raden D., and Kaufman R.J. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol. 4 (2006) e374 10.1371/journal.pbio.0040374
35. Scheuner D., Song B., McEwen E., Liu C., Laybutt R., Gillespie P., Saunders T., Bonner-Weir S., and Kaufman R.J. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7 (2001) 1165-1176
36. Schuster-Gossler K., Lee A.W., Lerner C.P., Parker H.J., Dyer V.W., Scott V.E., Gossler A., and Conover J.C. Use of coisogenic host blastocysts for efficient establishment of germline chimeras with C57BL/6J ES cell lines. Biotechniques 31 (2001) 1022-1024, 1026
37. Seong E., Saunders T.L., Stewart C.L., and Burmeister M. To knockout in 129 or in C57BL/6: That is the question. Trends Genet. 20 (2004) 59-62
38. Shen J., Chen X., Hendershot L., and Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3 (2002) 99-111
39. Shen X., Ellis R.E., Lee K., Liu C.Y., Yang K., Solomon A., Yoshida H., Morimoto R., Kurnit D.M., Mori K., et al. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107 (2001) 893-903
40. Sifers R.N., Brashears-Macatee S., Kidd V.J., Muensch H., and Woo S.L. A frameshift mutation results in a truncated alpha 1-antitrypsin that is retained within the rough endoplasmic reticulum. J. Biol. Chem. 263 (1988) 7330-7335
41. Thuerauf D.J., Morrison L., and Glembotski C.C. Opposing roles for ATF6alpha and ATF6beta in endoplasmic reticulum stress response gene induction. J. Biol. Chem. 279 (2004) 21078-21084
42. Thuerauf D.J., Marcinko M., Belmont P.J., and Glembotski C.C. Effects of the isoform-specific characteristics of ATF6alpha and ATF6beta on ER stress response gene expression and cell viability. J. Biol. Chem. (2007) 10.1074/jbc.M701213200
43. Wang Y., Shen J., Arenzana N., Tirasophon W., Kaufman R.J., and Prywes R. Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J. Biol. Chem. 275 (2000) 27013-27020
44. Wu J., and Kaufman R.J. From acute ER stress to physiological roles of the Unfolded Protein Response. Cell Death Differ. 13 (2006) 374-384
45. Xu C., Bailly-Maitre B., and Reed J.C. Endoplasmic reticulum stress: Cell life and death decisions. J. Clin. Invest. 115 (2005) 2656-2664
46. Yamamoto K., Yoshida H., Kokame K., Kaufman R.J., and Mori K. Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J. Biochem. (Tokyo) 136 (2004) 343-350
47. Yan W., Frank C.L., Korth M.J., Sopher B.L., Novoa I., Ron D., and Katze M.G. Control of PERK eIF2alpha kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc. Natl. Acad. Sci. USA 99 (2002) 15920-15925
48. Ye J., Rawson R.B., Komuro R., Chen X., Dave U.P., Prywes R., Brown M.S., and Goldstein J.L. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6 (2000) 1355-1364
49. Yoshida H., Haze K., Yanagi H., Yura T., and Mori K. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J. Biol. Chem. 273 (1998) 33741-33749
50. 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
51. 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
52. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., Stevens J.L., and Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12 (1998) 982-995