Toll-like receptor activation suppresses ER stress factor CHOP and translation inhibition through activation of eIF2B

Nature Cell Biology

Volumn 14, Issue 2, 2012, Pages 192-200

  Woo, Connie W ^a   Kutzler, Lydia ^b   Kimball, Scot R ^b   Tabas, Ira ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INITIATION FACTOR 2ALPHA; PHOSPHOPROTEIN PHOSPHATASE 2; PROTEIN TYROSINE KINASE; SERINE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TYROSINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CATALYSIS; CONTROLLED STUDY; DEPHOSPHORYLATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; UNFOLDED PROTEIN RESPONSE;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELLS, CULTURED; EMBRYO, MAMMALIAN; ENDOPLASMIC RETICULUM STRESS; EUKARYOTIC INITIATION FACTOR-2B; FIBROBLASTS; IMMUNOBLOTTING; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN PHOSPHATASE 2; RNA INTERFERENCE; SERINE; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION FACTOR CHOP; TUNICAMYCIN; UNFOLDED PROTEIN RESPONSE;

EID: 84856487878     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2408     Document Type: Article

References (41)

1. Todd, D. J., Lee, A. H. & Glimcher, L. H. The endoplasmic reticulum stress response in immunity and autoimmunity. Nat. Rev. Immunol. 8, 663-674 (2008).
2. Ron, D. & Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529 (2007). (Pubitemid 46985379)
3. Woo, C. W. et al. Adaptive suppression of the ATF4-CHOP branch of the unfolded protein response by toll-like receptor signalling. Nat. Cell Biol. 11, 1473-1480 (2009).
4. Ron, D. Translational control in the endoplasmic reticulum stress response. J. Clin. Invest. 110, 1383-1388 (2002). (Pubitemid 35396906)
5. Tabas, I. & Ron, D. Molecular mechanisms integrating pathways of endoplasmic reticulum stress-induced apoptosis. Nat. Cell Biol. 13, 184-190 (2011).
6. Oyadomari, S. & Mori, M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death. Differ. 11, 381-389 (2004). (Pubitemid 38489416)
7. Krishnamoorthy, T., Pavitt, G. D., Zhang, F., Dever, T. E. & Hinnebusch, A. G. Tight binding of the phosphorylatedαsubunit of initiation factor 2 (eIF2α) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol. Cell Biol. 21, 5018-5030 (2001). (Pubitemid 32656399)
8. Welsh, G. I., Miller, C. M., Loughlin, A. J., Price, N. T. & Proud, C. G. Regulation of eukaryotic initiation factor eIF2B: glycogen synthase kinase-3 phosphorylates a conserved serine which undergoes dephosphorylation in response to insulin. FEBS Lett. 421, 125-130 (1998). (Pubitemid 28288076)
9. Wang, X. & Proud, C. G. A novel mechanism for the control of translation initiation by amino acids, mediated by phosphorylation of eukaryotic initiation factor 2B. Mol. Cell Biol. 28, 1429-1442 (2008).
10. Hardt, S. E., Tomita, H., Katus, H. A. & Sadoshima, J. Phosphorylation of eukaryotic translation initiation factor 2Bεby glycogen synthase kinase-3βregulatesβ-adrenergic cardiac myocyte hypertrophy. Circ. Res. 94, 926-935 (2004). (Pubitemid 38490070)
11. Fang, X. et al. Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc. Natl Acad. Sci. USA 97, 11960-11965 (2000).
12. Chung, H., Nairn, A. C., Murata, K. & Brautigan, D. L. Mutation of Tyr307 and Leu309 in the protein phosphatase 2A catalytic subunit favors association with theα4 subunit which promotes dephosphorylation of elongation factor-2. Biochemistry 38, 10371-10376 (1999).
13. Evans, D. R., Myles, T., Hofsteenge, J. & Hemmings, B. A. Functional expression of human PP2Ac in yeast permits the identification of novel C-terminal and dominant-negative mutant forms. J. Biol. Chem. 274, 24038-24046 (1999).
14. Santa-Coloma, T. A. Anp32e (Cpd1) and related protein phosphatase 2 inhibitors. Cerebellum 2, 310-320 (2003). (Pubitemid 38280288)
15. Nanahoshi, M. et al.α4 protein as a common regulator of type 2A-related serine/threonine protein phosphatases. FEBS Lett. 446, 108-112 (1999). (Pubitemid 29127259)
16. Chen, J., Martin, B. L. & Brautigan, D. L. Regulation of protein serine-threonine phosphatase type-2A by tyrosine phosphorylation. Science 257, 1261-1264 (1992).
17. Hu, X. et al. Src kinase up-regulates the ERK cascade through inactivation of protein phosphatase 2A following cerebral ischemia. BMC. Neurosci. 10, 74 (2009).
18. Barisic, S., Schmidt, C., Walczak, H. & Kulms, D. Tyrosine phosphatase inhibition triggers sustained canonical serine-dependent NfiB activation via Src-dependent blockade of PP2A. Biochem. Pharmacol. 80, 439-447 (2010).
19. Brown, M. T. & Cooper, J. A. Regulation, substrates and functions of src. Biochim. Biophys. Acta 1287, 121-149 (1996).
20. Liu, X. et al. Regulation of c-Src tyrosine kinase activity by the Src SH2 domain. Oncogene 8, 1119-1126 (1993). (Pubitemid 23129833)
21. Lu, B. et al. Peptide neurotransmitters activate a cation channel complex of NALCN and UNC-80. Nature 457, 741-744 (2009).
22. Encinas, M. et al. c-Src is required for glial cell line-derived neurotrophic factor (GDNF) family ligand-mediated neuronal survival via a phosphatidylinositol-3 kinase (PI-3K)-dependent pathway. J. Neurosci. 21, 1464-1472 (2001). (Pubitemid 32182188)
23. Mayhew, D. L., Hornberger, T. A., Lincoln, H. C. & Bamman, M. M. Eukaryotic initiation factor 2Binduces cap-dependent translation and skeletal muscle hypertrophy. J. Physiol. 589, 3023-3037 (2011).
24. Potter, M. W., Shah, S. A., Elbirt, K. K. & Callery, M. P. Endotoxin (LPS) stimulates 4E-BP1/PHAS-I phosphorylation in macrophages. J. Surg. Res. 97, 54-59 (2001). (Pubitemid 34948219)
25. Lee, J. Y. et al. The regulation of the expression of inducible nitric oxide synthase by Src-family tyrosine kinases mediated through MyD88-independent signaling pathways of Toll-like receptor 4. Biochem. Pharmacol. 70, 1231-1240 (2005). (Pubitemid 41317517)
26. Kim, J. Y. et al. Src-mediated regulation of in flammatory responses by actin polymerization. Biochem. Pharmacol. 79, 431-443 (2010).
27. Tu, S., Wu, W. J., Wang, J. & Cerione, R. A. Epidermal growth factor-dependent regulation of Cdc42 is mediated by the Src tyrosine kinase. J. Biol. Chem. 278, 49293-49300 (2003).
28. Moore, K. J. & Tabas, I. Macrophages in the pathogenesis of atherosclerosis. Cell 145, 341-355 (2011).
29. Curtiss, L. K. & Tobias, P. S. Emerging role of toll-like receptors in atherosclerosis. J. Lipid Res. 50 Suppl, S340-S345 (2008).
30. Lee, A. S. & Hendershot, L. M. ER stress and cancer. Cancer Biol. Ther. 5, 721-722 (2006). (Pubitemid 44775123)
31. Check, J. et al. Src kinase participates in LPS-induced activation of NADPH oxidase. Mol. Immunol. 47, 756-762 (2010).
32. Healy, S. J., Gorman, A. M., Mousavi-Shafaei, P., Gupta, S. & Samali, A. Targeting the endoplasmic reticulum-stress response as an anticancer strategy. Eur. J. Pharmacol. 625, 234-246 (2009).
33. Cook, A. D., Braine, E. L. & Hamilton, J. A. The phenotype of in flammatory macrophages is stimulus dependent: implications for the nature of the in flammatory response. J. Immunol. 171, 4816-4823 (2003). (Pubitemid 37310602)
34. Zinszner, H. et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12, 982-995 (1998). (Pubitemid 28204605)
35. Jefferson, L. S., Fabian, J. R. & Kimball, S. R. Glycogen synthase kinase-3 is the predominant insulin-regulated eukaryotic initiation factor 2B kinase in skeletal muscle. Int. J. Biochem. Cell Biol. 31, 191-200 (1999). (Pubitemid 29094799)
36. Tuckow, A. P., Vary, T. C., Kimball, S. R. & Jefferson, L. S. Ectopic expression of eIF2Bin rat skeletal muscle rescues the sepsis-induced reduction in guanine nucleotide exchange activity and protein synthesis. Am. J. Physiol. Endocrinol. Metab. 299, E241-E248 (2010).
37. Novoa, I., Zeng, H., Harding, H. P. & Ron, D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol. 153, 1011-1022 (2001).
38. Feng, B. et al. The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat. Cell Biol. 5, 781-792 (2003). (Pubitemid 37087166)
39. Kimball, S. R., Everson, W. V., Flaim, K. E. & Jefferson, L. S. Initiation of protein synthesis in a cell-free system prepared from rat hepatocytes. Am. J. Physiol. 256, C28-C34 (1989).
40. Rowlands, A. G., Montine, K. S., Henshaw, E. C. & Panniers, R. Physiological stresses inhibit guanine-nucleotide-exchange factor in Ehrlich cells. Eur. J. Biochem. 175, 93-99 (1988).
41. Matts, R. L. & London, I. M. The regulation of initiation of protein synthesis by phosphorylation of eIF-2(α) and the role of reversing factor in the recycling of eIF-2. J. Biol. Chem. 259, 6708-6711 (1984). (Pubitemid 14078962)