Protein misfolding induces hypoxic preconditioning via a subset of the unfolded protein response machinery

Molecular and Cellular Biology

Volumn 30, Issue 21, 2010, Pages 5033-5042

  Mao, Xianrong R ^a   Crowder, C Michael ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; INITIATION FACTOR 2ALPHA; PROTEIN; PROTEIN GCN 2; PROTEIN IRE 1; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; CAENORHABDITIS ELEGANS PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; IRE-1 PROTEIN, C ELEGANS; PRIMER DNA; PROTEIN SERINE THREONINE KINASE;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; HYPOXIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TRANSLATION REGULATION; UNFOLDED PROTEIN RESPONSE; ANIMAL; ANOXIA; BIOLOGICAL MODEL; CHEMISTRY; DRUG EFFECTS; GENE; GENETICS; ISCHEMIC PRECONDITIONING; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; TRANSGENIC ANIMAL;

CAENORHABDITIS ELEGANS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANOXIA; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA PRIMERS; GENES, HELMINTH; GREEN FLUORESCENT PROTEINS; ISCHEMIC PRECONDITIONING; MODELS, BIOLOGICAL; MUTATION; PROTEIN FOLDING; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; TUNICAMYCIN; UNFOLDED PROTEIN RESPONSE;

EID: 77957826835     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00922-10     Document Type: Article

References (60)

1. Anderson, L. L., X. Mao, B. A. Scott, and C. M. Crowder. 2009. Survival from hypoxia in C. elegans by inactivation of aminoacyl-tRNA synthetases. Science 323:630-633.
2. Azfer, A., J. Niu, L. M. Rogers, F. M. Adamski, and P. E. Kolattukudy. 2006. Activation of endoplasmic reticulum stress response during the development of ischemic heart disease. Am. J. Physiol. Heart Circ. Physiol. 291:H1411-H1420.
3. Bernales, S., K. L. McDonald, and P. Walter. 2006. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 4:e423.
4. Bi, M., C. Naczki, M. Koritzinsky, D. Fels, J. Blais, N. Hu, H. Harding, I. Novoa, M. Varia, J. Raleigh, D. Scheuner, R. J. Kaufman, J. Bell, D. Ron, B. G. Wouters, and C. Koumenis. 2005. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 24:3470-3481.
5. Bischof, L. J., C. Y. Kao, F. C. Los, M. R. Gonzalez, Z. Shen, S. P. Briggs, F. G. van der Goot, and R. V. Aroian. 2008. Activation of the unfolded protein response is required for defenses against bacterial pore-forming toxin in vivo. PLoS Pathog. 4:e1000176.
6. Bolli, R. 2007. Preconditioning: a paradigm shift in the biology of myocardial ischemia. Am. J. Physiol. Heart Circ. Physiol. 292:H19-H27.
7. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
8. Calfon, M., H. Zeng, F. Urano, J. H. Till, S. R. Hubbard, H. P. Harding, S. G. Clark, and D. Ron. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92-96. (Pubitemid 34062456)
9. Caruso, M. E., S. Jenna, M. Bouchecareilh, D. L. Baillie, D. Boismenu, D. Halawani, M. Latterich, and E. Chevet. 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.
10. Dasgupta, N., A. M. Patel, B. A. Scott, and C. M. Crowder. 2007. Hypoxic preconditioning requires the apoptosis protein CED-4 in C. elegans. Curr. Biol. 17:1954-1959.
11. DeGracia, D. J. 2004. Acute and persistent protein synthesis inhibition following cerebral reperfusion. J. Neurosci. Res. 77:771-776.
12. Dirnagl, U., K. Becker, and A. Meisel. 2009. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol. 8:398-412.
13. Doroudgar, S., D. J. Thuerauf, M. C. Marcinko, P. J. Belmont, and C. C. Glembotski. 2009. Ischemia activates the ATF6 branch of the endoplasmic reticulum (ER) stress response. J. Biol. Chem. 284:29735-29745.
14. Edgley, M. L., and D. L. Riddle. 2001. LG II balancer chromosomes in Caenorhabditis elegans: mT1(II;III) and the mIn1 set of dominantly and recessively marked inversions. Mol. Genet. Genomics 266:385-395.
15. Han, D., A. G. Lerner, L. Vande Walle, J.-P. Upton, W. Xu, A. Hagen, B. J. Backes, S. A. Oakes, and F. R. Papa. 2009. IRE1α kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138:562-575.
16. Harding, H. P., I. Novoa, Y. Zhang, H. Zeng, R. Wek, M. Schapira, and D. Ron. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099-1108.
17. Hayashi, T., A. Saito, S. Okuno, M. Ferrand-Drake, and P. H. Chan. 2003. Induction of GRP78 by ischemic preconditioning reduces endoplasmic reticulum stress and prevents delayed neuronal cell death. J. Cereb. Blood Flow Metab. 23:949-961.
18. Hayashi, T., A. Saito, S. Okuno, M. Ferrand-Drake, R. L. Dodd, T. Nishi, C. M. Maier, H. Kinouchi, and P. H. Chan. 2003. Oxidative damage to the endoplasmic reticulum is implicated in ischemic neuronal cell death. J. Cereb. Blood Flow Metab. 23:1117-1128.
19. Hetz, C., and L. H. Glimcher. 2009. Fine-tuning of the unfolded protein response: assembling the IRE1α interactome. Mol. Cell 35:551-561.
20. Hollien, J., J. H. Lin, H. Li, N. Stevens, P. Walter, and J. S. Weissman. 2009. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 186:323-331.
21. Hollien, J., and J. S. Weissman. 2006. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313:104-107.
22. Kapulkin, W. J., B. G. Hiester, and C. D. Link. 2005. Compensatory regulation among ER chaperones in C. elegans. FEBS Lett. 579:3063-3068.
23. Kim, I., C. W. Shu, W. Xu, C. W. Shiau, D. Grant, S. Vasile, N. D. Cosford, and J. C. Reed. 2009. Chemical biology investigation of cell death pathways activated by endoplasmic reticulum stress reveals cytoprotective modulators of ASK1. J. Biol. Chem. 284:1593-1603.
24. Koumenis, C., M. Bi, J. Ye, D. Feldman, and A. C. Koong. 2007. Hypoxia and the unfolded protein response. Methods Enzymol. 435:275-293.
25. Koumenis, C., C. Naczki, M. Koritzinsky, S. Rastani, A. Diehl, N. Sonenberg, A. Koromilas, and B. G. Wouters. 2002. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol. Cell. Biol. 22:7405-7416.
26. Lee, K., W. Tirasophon, X. Shen, M. Michalak, R. Prywes, T. Okada, H. Yoshida, K. Mori, and R. J. Kaufman. 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.
27. Luo, D., Y. He, H. Zhang, L. Yu, H. Chen, Z. Xu, S. Tang, F. Urano, and W. Min. 2008. AIP1 is critical in transducing IRE1-mediated endoplasmic reticulum stress response. J. Biol. Chem. 283:11905-11912.
28. Martindale, J. J., R. Fernandez, D. Thuerauf, R. Whittaker, N. Gude, M. A. Sussman, and C. C. Glembotski. 2006. Endoplasmic reticulum stress gene induction and protection from ischemia/reperfusion injury in the hearts of transgenic mice with a tamoxifen-regulated form of ATF6. Circ. Res. 98:1186-1193.
29. Merksamer, P. I., A. Trusina, and F. R. Papa. 2008. Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions. Cell 135:933-947.
30. Murry, C. E., R. B. Jennings, and K. A. Reimer. 1986. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124-1136.
31. Nagai, A., H. Kadowaki, T. Maruyama, K. Takeda, H. Nishitoh, and H. Ichijo. 2009. USP14 inhibits ER-associated degradation via interaction with IRE1alpha. Biochem. Biophys. Res. Commun. 379:995-1000.
32. Nishitoh, H., A. Matsuzawa, K. Tobiume, K. Saegusa, K. Takeda, K. Inoue, S. Hori, A. Kakizuka, and H. Ichijo. 2002. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 16:1345-1355.
33. Nukazuka, A., H. Fujisawa, T. Inada, Y. Oda, and S. Takagi. 2008. Semaphorin controls epidermal morphogenesis by stimulating mRNA translation via eIF2α in Caenorhabditis elegans. Genes Dev. 22:1025-1036. (Pubitemid 351544241)
34. Obrenovitch, T. P. 2008. Molecular physiology of preconditioning-induced brain tolerance to ischemia. Physiol. Rev. 88:211-247.
35. Ogata, M., S. Hino, A. Saito, K. Morikawa, S. Kondo, S. Kanemoto, T. Murakami, M. Taniguchi, I. Tanii, K. Yoshinaga, S. Shiosaka, J. A. Hammarback, F. Urano, and K. Imaizumi. 2006. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell. Biol. 26:9220-9231.
36. Oh, S. W., A. Mukhopadhyay, N. Svrzikapa, F. Jiang, R. J. Davis, and H. A. Tissenbaum. 2005. JNK regulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16. Proc. Natl. Acad. Sci. U. S. A. 102:4494-4499.
37. Oikawa, D., M. Tokuda, and T. Iwawaki. 2007. Site-specific cleavage of CD59 mRNA by endoplasmic reticulum-localized ribonuclease, IRE1. Biochem. Biophys. Res. Commun. 360:122-127.
38. Oyadomari, S., and M. Mori. 2004. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11:381-389.
39. Paschen, W., C. Aufenberg, S. Hotop, and T. Mengesdorf. 2003. Transient cerebral ischemia activates processing of xbp1 messenger RNA indicative of endoplasmic reticulum stress. J. Cereb. Blood Flow Metab. 23:449-461.
40. Patil, C. K., H. Li, and P. Walter. 2004. Gcn4p and novel upstream activating sequences regulate targets of the unfolded protein response. PLoS Biol. 2:E246.
41. Prachasilchai, W., H. Sonoda, N. Yokota-Ikeda, S. Oshikawa, C. Aikawa, K. Uchida, K. Ito, T. Kudo, K. Imaizumi, and M. Ikeda. 2008. A protective role of unfolded protein response in mouse ischemic acute kidney injury. Eur. J. Pharmacol. 592:138-145.
42. Quinones, Q. J., G. G. de Ridder, and S. V. Pizzo. 2008. GRP78: a chaperone with diverse roles beyond the endoplasmic reticulum. Histol. Histopathol. 23:1409-1416.
43. Roberts, G. G., M. J. Di Loreto, M. Marshall, J. Wang, and D. J. DeGracia. 2007. Hippocampal cellular stress responses after global brain ischemia and reperfusion. Antioxid. Redox. Signal 9:2265-2275.
44. Rzymski, T., and A. L. Harris. 2007. The unfolded protein response and integrated stress response to anoxia. Clin. Cancer Res. 13:2537-2540.
45. Samokhvalov, V., B. A. Scott, and C. M. Crowder. 2008. Autophagy protects against hypoxic injury in C. elegans. Autophagy 4:1034-1041.
46. Sasagawa, Y., K. Yamanaka, and T. Ogura. 2007. ER E3 ubiquitin ligase HRD-1 and its specific partner chaperone BiP play important roles in ERAD and developmental growth in Caenorhabditis elegans. Genes Cells 12:1063-1073. (Pubitemid 47365677)
47. Scott, B. A., M. S. Avidan, and C. M. Crowder. 2002. Regulation of hypoxic death in C. elegans by the insulin/IGF receptor homolog DAF-2. Science 296:2388-2391.
48. Shen, X., R. E. Ellis, K. Lee, C. Y. Liu, K. Yang, A. Solomon, H. Yoshida, R. Morimoto, D. M. Kurnit, K. Mori, and R. J. Kaufman. 2001. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107:893-903.
49. Shen, X., R. E. Ellis, K. Sakaki, and R. J. Kaufman. 2005. Genetic interactions due to constitutive and inducible gene regulation mediated by the unfolded protein response in C. elegans. PLoS Genet. 1:e37.
50. Shim, J., T. Umemura, E. Nothstein, and C. Rongo. 2004. The unfolded protein response regulates glutamate receptor export from the endoplasmic reticulum. Mol. Biol. Cell 15:4818-4828.
51. Sommerschild, H. T., and K. A. Kirkeboen. 2002. Preconditioning- endogenous defence mechanisms of the heart. Acta Anaesthesiol. Scand. 46:123-137.
52. Stiernagle, T. 11 February 2006, posting date. Maintenance of C. elegans. In D. Fay (ed.), Wormbook. The C. elegans Research Community. doi:10.1895/wormbook.1.101.1.
53. Tajiri, S., S. Oyadomari, S. Yano, M. Morioka, T. Gotoh, J. I. Hamada, Y. Ushio, and M. Mori. 2004. Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ. 11:403-415.
54. Truettner, J. S., K. Hu, C. L. Liu, W. D. Dietrich, and B. Hu. 2009. Subcellular stress response and induction of molecular chaperones and folding proteins after transient global ischemia in rats. Brain Res. 1249:9-18.
55. Uccelletti, D., A. Pascoli, F. Farina, A. Alberti, P. Mancini, C. B. Hirschberg, and A. C. Palleschi. 2008. APY-1, a novel Caenorhabditis elegans apyrase involved in unfolded protein response signalling and stress responses. Mol. Biol. Cell 19:1337-1345.
56. Urano, F., X. Wang, A. Bertolotti, Y. Zhang, P. Chung, H. P. Harding, and D. Ron. 2000. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664-666. (Pubitemid 30070916)
57. Wang, S., F. M. Longo, J. Chen, M. Butman, S. H. Graham, K. G. Haglid, and F. R. Sharp. 1993. Induction of glucose regulated protein (grp78) and inducible heat shock protein (hsp70) mRNAs in rat brain after kainic acid seizures and focal ischemia. Neurochem. Int. 23:575-582.
58. Yamamoto, K., T. Sato, T. Matsui, M. Sato, T. Okada, H. Yoshida, A. Harada, and K. Mori. 2007. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev. Cell 13:365-376.
59. Yamamoto, K., H. Yoshida, K. Kokame, R. J. Kaufman, and K. Mori. 2004. Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J. Biochem. 136:343-350. (Pubitemid 39545794)
60. Yoshida, H., T. Matsui, A. Yamamoto, T. Okada, and K. Mori. 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.