Phosphorylation of eIF2α in response to 26S proteasome inhibition is mediated by the haem-regulated inhibitor (HRI) kinase

Biochemical Journal

Volumn 412, Issue 3, 2008, Pages 579-588

  Yerlikaya, Azmi ^a   Kimball, Scot R ^b   Stanley, Bruce A ^b  

^a DUMLUPINAR UNIVERSITY   (Turkey)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

26S proteasome; Apoptosis; Eukaryotic translational initiation factor 2 (eIF2 ); Protein degradation; Protein kinase; Protein synthesis

Indexed keywords

CELL CULTURE; CELL DEATH; CELLS; MAGNESIUM PRINTING PLATES; MAN MACHINE SYSTEMS; NUCLEIC ACIDS; PHOSPHORYLATION; RNA; SULFATE MINERALS;

26 S PROTEASOME; AFTER-TREATMENT; APOPTOSIS; CELL LINES; CONTROL CELLS; ENDOPLASMIC RETICULUM (EI); GENERAL (CO); PROTEASOME INHIBITORS; PROTEIN SYNTHESIS; RNA DEPENDENT PROTEIN KINASE (PKR); TRANSLATIONAL INITIATION;

CHEMICAL REACTIONS;

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; EUKARYOTIC TRANSLATION INITIATION FACTOR 2ALPHA; INITIATION FACTOR 2ALPHA; KINASE GCN2; KINASE HRI; KINASE PERK; PHOSPHOTRANSFERASE; PROTEASE 26 S; PROTEIN KINASE; PROTEINASE; ATP DEPENDENT 26S PROTEASE; INITIATION FACTOR 2; PROTEASOME; PROTEIN KINASE R; PROTEINASE INHIBITOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL LINE; CONTROLLED STUDY; ENZYME INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; ANIMAL; CELL STRAIN COS1; CERCOPITHECUS; DRUG ANTAGONISM; METABOLISM; PHOSPHORYLATION;

EUKARYOTA;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; EIF-2 KINASE; EUKARYOTIC INITIATION FACTOR-2; MICE; PHOSPHORYLATION; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX;

EID: 45349091778     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20080324     Document Type: Article

References (50)

1. Hershey, J. W. (1991) Translational control in mammalian cells. Annu. Rev. Biochem. 60, 717-755
2. Kimball, S. R. (1999) Eukaryotic initiation factor eIF2. Int. J. Biochem. Cell Biol. 31, 25-29
3. Satoh, S., Hijikata, M., Handa, H. and Shimotohno, K. (1999) Caspase-mediated cleavage of eukaryotic translation initiation factor subunit 2α. Biochem. J. 342, 65-70
4. Pain, V. M. (1996) Initiation of protein synthesis in eukaryotic cells. Eur. J. Biochem. 236, 747-771
5. Marissen, W. E., Guo, Y., Thomas, A. A., Matts, R. L. and Lloyd, R. E. (2000) Identification of caspase 3-mediated cleavage and functional alteration of eukaryotic initiation factor 2α in apoptosis. J. Biol. Chem. 275, 9314-9323
6. Kumar, K. U., Srivastava, S. P. and Kaufman, R. J. (1999) Double-stranded RNA-activated protein kinase (PKR) is negatively regulated by 60S ribosomal subunit protein L18. Mol. Cell. Biol. 19, 1116-1125
7. -/- mice reveals a role for translational control in secretory cell survival. Mol. Cell 7, 1153-1163
8. Hilt, W. and Wolf, D. H. (1996) Proteasomes: destruction as a programme. Trends Biochem. Sci. 21, 96-102
9. Schubert, U., Anton, L. C., Gibbs, J., Norbury, C. C., Yewdell, J. W. and Bennink, J. R. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404, 770-774
10. Mimnaugh, E. G., Chen, H. Y., Davie, J. R., Celis, J. E. and Neckers, L. (1997) Rapid deubiquitination of nucleosomal histones in human tumor cells caused by proteasome inhibitors and stress response inducers: effects on replication, transcription, translation, and the cellular stress response. Biochemistry 36, 14418-14429
11. Jiang, H. Y. and Wek, R. C. (2005) Phosphorylation of the α-subunit of the eukaryotic initiation factor-2 (eIF2α) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J. Biol. Chem. 280, 14189-14202
12. Bush, K. T., Goldberg, A. L. and Nigam, S. K. (1997) Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance. J. Biol. Chem. 272, 9086-9092
13. Yerlikaya, A. and Stanley, B. A. (2004) S- adenosylmethionine decarboxylase degradation by the 26 S proteasome is accelerated by substrate-mediated transamination. J. Biol. Chem. 279, 12469-12478
14. Pasquini, L. A., Besio Moreno, M., Adamo, A. M., Pasquini, J. M. and Soto, E. F. (2000) Lactacystin, a specific inhibitor of the proteasome, induces apoptosis and activates caspase-3 in cultured cerebellar granule cells. J. Neurosci. Res. 59, 601-611
15. Wagenknecht, B., Hermisson, M., Eitel, K. and Weller, M. (1999) Proteasome inhibitors induce p53/p21-independent apoptosis in human glioma cells. Cell. Physiol. Biochem. 9, 117-125
16. Drexler, H. C. (1997) Activation of the cell death program by inhibition of proteasome function. Proc. Natl. Acad. Sci. U.S.A. 94, 855-860
17. Giuliano, M., Lauricella, M., Calvaruso, G., Carabillo, M., Emanuele, S., Vento, R. and Tesoriere, G. (1999) The apoptotic effects and synergistic interaction of sodium butyrate and MG132 in human retinoblastoma Y79 cells. Cancer Res. 59, 5586-5595
18. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
19. Freshney, R. I. (1994) Culture of Animal Cells: A Manual of Basic Techniques, Wiley-Liss, New York
20. Vermes, I., Haanen, C., Steffens-Nakken, H. and Reutelingsperger, C. (1995) A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods 184, 39-51
21. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
22. Naujokat, C., Sezer, O., Zinke, H., Leclere, A., Hauptmann, S. and Possinger, K. (2000) Proteasome inhibitors induced caspase-dependent apoptosis and accumulation of p21WAF1/Cip1 in human immature leukemic cells. Eur. J. Haematol. 65, 221-236
23. Drexler, H. C., Risau, W. and Konerding, M. A. (2000) Inhibition of proteasome function induces programmed cell death in proliferating endothelial cells. FASEB J. 14, 65-77
24. Marissen, W. E. and Lloyd, R. E. (1998) Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol. Cell. Biol. 18, 7565-7574
25. Etchison, D., Milburn, S. C., Edery, I., Sonenberg, N. and Hershey, J. W. (1982) Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex. J. Biol. Chem. 257, 14806-14810
26. Babu, S. V. and Ramaiah, K. V. (1996) Type 1 phosphatase inhibitors reduce the restoration of guanine nucleotide exchange activity of eukaryotic initiation factor 2B inhibited reticulocyte lysates rescued by hemin. Arch. Biochem. Biophys. 327, 201-208
27. Redpath, N. T. and Proud, C. G. (1990) Activity of protein phosphatases against initiation factor-2 and elongation factor-2. Biochem. J. 272, 175-180
28. Williams, B. R. (1999) PKR: a sentinel kinase for cellular stress. Oncogene 18, 6112-6120
29. Hershko, A. and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479
30. Kaufman, R. J. (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13, 1211-1233
31. 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
32. Brewer, J. W. and Diehl, J. A. (2000) PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc. Natl. Acad. Sci. U.S.A. 97, 12625-12630
33. Chen, J. J. and London, I. M. (1995) Regulation of protein synthesis by heme-regulated eIF-2α kinase. Trends Biochem. Sci. 20, 105-108
34. Zhou, J., Köhl, R., Herr, B., Frank, R. and Brüne, B. (2006) Calpain mediates a von Hippel-Lindau protein-independent destruction of hypoxia-inducible factor-1. Mol. Biol. Cell 15, 1549-1558
35. Lee, D. H. and Goldberg, A. L. (1998) Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8, 397-403
36. Adams, J., Palombella, V. J., Sausville, E. A., Johnson, J., Destree, A., Lazarus, D. D., Maas, J., Pien, C. S., Prakash, S. and Elliot, P. J. (1999) Proteasome inhibitors: a novel class of potent and effective antitumor agents. Cancer Res. 59, 2615-2622
37. Tanaka, K. (1998) Molecular biology of the proteasome. Biochem. Biophys. Res. Commun. 247, 537-541
38. Cowan, J. L. and Morley, S. J. (2004) The proteasome inhibitor, MG132, promotes the reprogramming of translation in C2C12 myoblasts and facilitates the association of hsp25 with the eIF4F complex. Eur. J. Biochem. 271, 3596-3611
39. Wagenknecht, B., Hermisson, M., Groscurth, P., Liston, P., Krammer, P. H. and Weller, M. (2000) Proteasome inhibitor-induced apoptosis of glioma cells involves the processing of multiple caspases and cytochrome c release. J. Neurochem. 75, 2288-2297
40. Brophy, V. A., Tavare, J. M. and Rivett, A. J. (2002) Treatment of COS-7 cells with proteasome inhibitors or gamma-interferon reduces the increase in caspase 3 activity associated with staurosporine-induced apoptosis. Arch. Biochem. Biophys. 397, 199-205
41. Berlanga, J. J., Herrero, S. and de Haro, C. (1998) Characterization of the hemin-sensitive eukaryotic initiation factor 2α kinase from mouse non-erythroid cells. J. Biol. Chem. 273, 32340-32346
42. Mellor, H., Flowers, K. M., Kimball, S. R. and Jefferson, L. S. (1994) Cloning and characterization of cDNA encoding rat hemin-sensitive initiation factor-2α (eIF-2α) kinase. Evidence for multi-tissue expression. J. Biol. Chem. 269, 10201-10204
43. + channel blocker aprindine. Biochem. Biophys. Res. Commun. 331, 1001-1006
44. Alao, J. P., Stavropoulou, A. V., Lam, E. W.-F., Coombes, R. C. and Vigushin, D. M. (2006) Histone deacetylase inhibitor, trichostatin A induces ubiquitin-dependent cyclin D1 degradation in MCF-7 breast cancer cells. Mol. Cancer 5, 8
45. Kim, D., Kim, S. H. and Li, G. C. (1999) Proteasome inhibitors MG132 and lactacystin hyperphosphorylate HSF1 and induce hsp70 and hsp27 expression. Biochem. Biophys. Res. Commun. 254, 264-268
46. Awasthi, N. and Wagner, B. J. (2005) Upregulation of heat shock protein expression by proteasome inhibition: an anti-apoptotic mechanism in the lens. Invest. Ophthalmol. Vis. Sci. 46, 2082-2091
47. Lu, L., Han, A. P. and Chen, J. J. (2001) Translation initiation control by heme-regulated eukaryotic initiation factor 2α kinase in erythroid cells under cytoplasmic stresses. Mol. Cell. Biol. 21, 7971-7980
48. Adams, J. (2004) The development of proteasome inhibitors as anticancer drugs. Cancer Cell 5, 417-421
49. Richardson, P. G., Barlogie, B., Berenson, J., Singhal, S., Jagannath, S., Irwin, D., Rajkumar, S. V., Srkalovic, G., Alsina, M., Alexanian, R. et al. (2003) A phase 2 study of Bortezomib in relapsed, refractory myeloma. N. Engl. J. Med. 348, 2609-2617
50. Jones, E. L., Zhao, M. J., Stevenson, M. A. and Calderwood, S. K. (2004) The 70 kilodalton heat shock protein is an inhibitor of apoptosis in prostate cancer. Int. J. Hyperthermia 20, 835-849