Implication of eIF2α kinase GCN2 in induction of apoptosis and endoplasmic reticulum stress-responsive genes by sodium salicylate

Journal of Pharmacy and Pharmacology

Volumn 65, Issue 3, 2013, Pages 430-440

  Gentz, Solange H L ^a   Bertollo, Caryne M ^b   Souza Fagundes, Elaine M ^a   Da Silva, Aristóbolo Mendes ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

apoptosis; endoplasmic reticulum; kinase; mRNA translation; sodium salicylate

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; ACTIVATING TRANSCRIPTION FACTOR 6; INITIATION FACTOR 2ALPHA; LIPOCORTIN 5; PROPIDIUM IODIDE; PROTEIN KINASE; PROTEIN KINASE GENERAL CONTROL NON-DEREPRESSIBLE 2; S 3007; SALICYLATE SODIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL VIABILITY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENDOPLASMIC RETICULUM STRESS-RESPONSIVE GENE; FIBROBLAST; GENE; GENE EXPRESSION; GENE FUNCTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; WESTERN BLOTTING; WILD TYPE;

ACTIVATING TRANSCRIPTION FACTOR 6; ANIMALS; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; FIBROBLASTS; GENE EXPRESSION; MICE; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; SODIUM SALICYLATE; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION, GENETIC;

EID: 84873091064     PISSN: 00223573     EISSN: 20427158     Source Type: Journal    
DOI: 10.1111/jphp.12002     Document Type: Article

References (58)

1. Reid J, et al. Aspirin and diabetes mellitus. Br Med J 1957; 2: 1071-1074.
2. Tegeder I, et al. Cyclooxygenase-independent actions of cyclooxygenase inhibitors. FASEB J 2001; 15: 2057-2072.
3. Shoelson SE, et al. Inflammation and the IKK beta/I kappa B/NF-kappa B axis in obesity- and diet-induced insulin resistance. Int J Obes Relat Metab Disord 2003; 27 (Suppl. 3): S49-S52.
4. Amann R, Peskar BA,. Anti-inflammatory effects of aspirin and sodium salicylate. Eur J Pharmacol 2002; 447: 1-9.
5. Vane JR,. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol 1971; 231: 232-235.
6. Preston SJ, et al. Comparative analgesic and anti-inflammatory properties of sodium salicylate and acetylsalicylic acid (aspirin) in rheumatoid arthritis. Br J Clin Pharmacol 1989; 27: 607-611.
7. Klampfer L, et al. Sodium salicylate activates caspases and induces apoptosis of myeloid leukemia cell lines. Blood 1999; 93: 2386-2394.
8. Schwenger P, et al. Sodium salicylate induces apoptosis via p38 mitogen-activated protein kinase but inhibits tumor necrosis factor-induced c-Jun N-terminal kinase/stress-activated protein kinase activation. Proc Natl Acad Sci U S A 1997; 94: 2869-2873.
9. Sotiriou C, et al. The aspirin metabolite salicylate inhibits breast cancer cells growth and their synthesis of the osteolytic cytokines interleukins-6 and -11. Anticancer Res 1999; 19 (4B): 2997-3006.
10. Kopp E, Ghosh S,. Inhibition of NF-kappa B by sodium salicylate and aspirin. Science 1994; 265: 956-959.
11. Pierce JW, et al. Salicylates inhibit I kappa B-α phosphorylation, endothelial-leukocyte adhesion molecule expression, and neutrophil transmigration. J Immunol 1996; 156: 3961-3969.
12. Schwenger P, et al. Cell-type-specific activation of c-Jun N-terminal kinase by salicylates. J Cell Physiol 1999; 179: 109-114.
13. Shoelson SE, et al. Inflammation and insulin resistance. J Clin Invest 2006; 116: 1793-1801.
14. Tuncman G, et al. Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc Natl Acad Sci U S A 2006; 103: 10741-10746.
15. Hotamisligil GS,. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010; 140: 900-917.
16. Zhang K, Kaufman RJ,. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008; 454: 455-462.
17. He B, et al. Effect of sodium salicylate on oxidative stress and insulin resistance induced by free fatty acids. Hepatobiliary Pancreat Dis Int 2010; 9: 49-53.
18. Marciniak SJ, Ron D,. Endoplasmic reticulum stress signaling in disease. Physiol Rev 2006; 86: 1133-1149.
19. Ron D, Walter P,. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8: 519-529.
20. Kaufman RJ,. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 1999; 13: 1211-1233.
21. Wiseman RL, et al. SnapShot: the unfolded protein response. Cell 2010; 140: 590-590.e2.
22. Calfon M, et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002; 415: 92-96.
23. Shaffer AL, et al. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 2004; 21: 81-93.
24. Tabas I, Ron D,. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 2011; 13: 184-190.
25. Harding HP, et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 2000; 6: 1099-1108.
26. Silva AM, et al. Salicylates trigger protein synthesis inhibition in a PKR-Like endoplasmic reticulum kinase-dependent manner. J Biol Chem 2007; 282: 10164-10171.
27. Hinnebusch AG,. Translational Control of Gene Expression. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2000, Sonenberg N, et al., eds.
28. Chen JJ, London IM,. Regulation of protein synthesis by heme-regulated eIF-2 α kinase. Trends Biochem Sci 1995; 20: 105-108.
29. Chen JJ,. Regulation of protein synthesis by the heme-regulated eIF2α kinase: relevance to anemias. Blood 2007; 109: 2693-2699.
30. Clemens MJ, Elia A,. The double-stranded RNA-dependent protein kinase PKR: structure and function. J Interferon Cytokine Res 1997; 17: 503-524.
31. Kaufman RJ,. Orchestrating the unfolded protein response in health and disease. J Clin Invest 2002; 110: 1389-1398.
32. Kimball SR,. Regulation of translation initiation by amino acids in eukaryotic cells. Prog Mol Subcell Biol 2001; 26: 155-184.
33. Wek RC, et al. Juxtaposition of domains homologous to protein kinases and histidyl-tRNA synthetases in GCN2 protein suggests a mechanism for coupling GCN4 expression to amino acid availability. Proc Natl Acad Sci U S A 1989; 86: 4579-4583.
34. Berlanga JJ, et al. Characterization of a mammalian homolog of the GCN2 eukaryotic initiation factor 2α kinase. Eur J Biochem 1999; 265: 754-762.
35. Deng J, et al. Activation of GCN2 in UV-irradiated cells inhibits translation. Curr Biol 2002; 12: 1279-1286.
36. Hamanaka RB, et al. PERK and GCN2 contribute to eIF2α phosphorylation and cell cycle arrest after activation of the unfolded protein response pathway. Mol Biol Cell 2005; 16: 5493-5501.
37. Pereira CM, et al. IMPACT, a protein preferentially expressed in the mouse brain, binds GCN1 and inhibits GCN2 activation. J Biol Chem 2005; 280: 28316-28323.
38. Alves VS, et al. GCN2 activation and eIF2α phosphorylation in the maturation of mouse oocytes. Biochem Biophys Res Commun 2009; 378: 41-44.
39. Gotoh T, et al. Nitric oxide-induced apoptosis in RAW 264.7 macrophages is mediated by endoplasmic reticulum stress pathway involving ATF6 and CHOP. J Biol Chem 2002; 277: 12343-12350.
40. Riccardi C, Nicoletti I,. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc 2006; 1: 1458-1461.
41. Ubeda M, Habener JF,. CHOP gene expression in response to endoplasmic-reticular stress requires NFY interaction with different domains of a conserved DNA-binding element. Nucleic Acids Res 2000; 28: 4987-4997.
42. Yoshida H, et al. 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 1998; 273: 33741-33749.
43. Shiff SJ, et al. Sulindac sulfide, an aspirin-like compound, inhibits proliferation, causes cell cycle quiescence, and induces apoptosis in HT-29 colon adenocarcinoma cells. J Clin Invest 1995; 96: 491-503.
44. Bunce CM, et al. Potentiation of myeloid differentiation by anti-inflammatory agents, by steroids and by retinoic acid involves a single intracellular target, probably an enzyme of the aldoketoreductase family. Biochim Biophys Acta 1996; 1311: 189-198.
45. Shiff SJ, et al. Nonsteroidal antiinflammatory drugs inhibit the proliferation of colon adenocarcinoma cells: effects on cell cycle and apoptosis. Exp Cell Res 1996; 222: 179-188.
46. Wei L, et al. Salicylate-induced degeneration of cochlea spiral ganglion neurons-apoptosis signaling. Neuroscience 2010; 168: 288-299.
47. Iglesias-Serret D, et al. Aspirin induces apoptosis in human leukemia cells independently of NF-kappaB and MAPKs through alteration of the Mcl-1/Noxa balance. Apoptosis 2010; 15: 219-229.
48. Masud A, et al. Endoplasmic reticulum stress-induced death of mouse embryonic fibroblasts requires the intrinsic pathway of apoptosis. J Biol Chem 2007; 282: 14132-14139.
49. Kanda H, Miura M,. Regulatory roles of JNK in programmed cell death. J Biochem 2004; 136: 1-6.
50. Mauro C, et al. Central role of the scaffold protein tumor necrosis factor receptor-associated factor 2 in regulating endoplasmic reticulum stress-induced apoptosis. J Biol Chem 2006; 281: 2631-2638.
51. Roy B, Lee AS,. The mammalian endoplasmic reticulum stress response element consists of an evolutionarily conserved tripartite structure and interacts with a novel stress-inducible complex. Nucleic Acids Res 1999; 27: 1437-1443.
52. Mori K,. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 2000; 101: 451-454.
53. Kim I, et al. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 2008; 7: 1013-1030.
54. McCullough KD, et al. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001; 21: 1249-1259.
55. Munn DH, et al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 2005; 22: 633-642.
56. Jiang HY, Wek RC,. 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 2005; 280: 14189-14202.
57. Morishima N, et al. Activating transcription factor-6 (ATF6) mediates apoptosis with reduction of myeloid cell leukemia sequence 1 (Mcl-1) via induction of WW domain binding protein 1. J Biol Chem 2011; 286: 35227-35235.
58. Hendriksen PJ, et al. Evolution of the androgen receptor pathway during progression of prostate cancer. Cancer Res 2006; 66: 5012-5020.