Protein phosphatase 2A promotes endothelial survival via stabilization of translational inhibitor 4E-BP1 following exposure to tumor necrosis factor-α

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 11, 2011, Pages 2586-2594

  Janzen, Carla ^a   Sen, Suvajit ^a   Cuevas, Janis ^a   Reddy, Srinivasa T ^a   Chaudhuri, Gautam ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

apoptosis; atherosclerosis; cytokines; endothelial function; endothelium

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CYCLOHEXIMIDE; INITIATION FACTOR 4E BINDING PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOPROTEIN PHOSPHATASE 2; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN STABILITY; SENSITIZATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; CYCLOHEXIMIDE; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; EUKARYOTIC INITIATION FACTOR-4E; HUMANS; IMIDAZOLES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOPROTEINS; PROTEIN PHOSPHATASE 2; PYRIDINES; RNA, SMALL INTERFERING; TUMOR NECROSIS FACTOR-ALPHA;

EID: 80054900189     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.230946     Document Type: Article

References (41)

1. Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol. 2007;7:803-815. (Pubitemid 47480307)
2. Choy JC, Granville DJ, Hunt DW, McManus BM. Endothelial cell apoptosis: biochemical characteristics and potential implications for atherosclerosis. J Mol Cell Cardiol. 2001;33:1673-1690. (Pubitemid 32844225)
3. Kavurma MM, Tan NY, Bennett MR. Death receptors and their ligands in atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28:1694-1702.
4. Pohlman TH, Harlan JM. Human endothelial cell response to lipopolysaccharide, interleukin-1, and tumor necrosis factor is regulated by protein synthesis. Cell Immunol. 1989;119:41-52. (Pubitemid 19080428)
5. Gratton JP, Morales-Ruiz M, Kureishi Y, Fulton D, Walsh K, Sessa WC. Akt down-regulation of p38 signaling provides a novel mechanism of vascular endothelial growth factor-mediated cytoprotection in endothelial cells. J Biol Chem. 2001;276:30359-30365.
6. Aggarwal BB. Signalling pathways of the TNF superfamily: a double-edged sword. Nat Rev Immunol. 2003;3:745-756. (Pubitemid 41070815)
7. Polunovsky VA, Wendt CH, Ingbar DH, Peterson MS, Bitterman PB. Induction of endothelial cell apoptosis by TNFα: modulation by inhibitors of protein synthesis. Exp Cell Res. 1994;214:584-594. (Pubitemid 24310817)
8. Obrig TG, Culp WJ, McKeehan WL, Hardesty B. The mechanism by which cycloheximide and related glutarimide antibiotics inhibit peptide synthesis on reticulocyte ribosomes. J Biol Chem. 1971;246:174-181.
9. Halvorsen B, Otterdal K, Dahl TB, Skjelland M, Gullestad L, Oie E, Aukrust P. Atherosclerotic plaque stability: what determines the fate of a plaque? Prog Cardiovasc Dis. 2008;51:183-194.
10. Croons V, Martinet W, Herman AG, Timmermans JP, De Meyer GR. Selective clearance of macrophages in atherosclerotic plaques by the protein synthesis inhibitor cycloheximide. J Pharmacol Exp Ther. 2007; 320:986-993. (Pubitemid 46294043)
11. Croons V, Martinet W, Herman AG, Timmermans JP, De Meyer GR. The protein synthesis inhibitor anisomycin induces macrophage apoptosis in rabbit atherosclerotic plaques through p38 mitogen-activated protein kinase. J Pharmacol Exp Ther. 2009;329:856-864.
12. Goodfellow IG, Roberts LO. Eukaryotic initiation factor 4E. Int J Biochem Cell Biol. 2008;40:2675-2680.
13. Dubois L, Magagnin MG, Cleven AH, Weppler SA, Grenacher B, Landuyt W, Lieuwes N, Lambin P, Gorr TA, Koritzinsky M, Wouters BG. Inhibition of 4E-BP1 sensitizes U87 glioblastoma xenograft tumors to irradiation by decreasing hypoxia tolerance. Int J Radiat Oncol Biol Phys. 2009;73:1219-1227.
14. Tee AR, Proud CG. Caspase cleavage of initiation factor 4E-binding protein 1 yields a dominant inhibitor of cap-dependent translation and reveals a novel regulatory motif. Mol Cell Biol. 2002;22:1674-1683. (Pubitemid 34174985)
15. Morley SJ, Coldwell MJ, Clemens MJ. Initiation factor modifications in the preapoptotic phase. Cell Death Differ. 2005;12:571-584. (Pubitemid 40774768)
16. Herbert TP, Fahraeus R, Prescott A, Lane DP, Proud CG. Rapid induction of apoptosis mediated by peptides that bind initiation factor eIF4E. Curr Biol. 2000;10:793-796. (Pubitemid 30466944)
17. Jaffe EA, Hoyer LW, Nachman RL. Synthesis of antihemophilic factor antigen by cultured human endothelial cells. J Clin Invest. 1973;52: 2757-2764.
18. Liu G, Zhang Y, Bode AM, Ma WY, Dong Z. Phosphorylation of 4E-BP1 is mediated by the p38/MSK1 pathway in response to UVB irradiation. J Biol Chem. 2002;277:8810-8816. (Pubitemid 34952946)
19. Morley SJ. Intracellular signalling pathways regulating initiation factor eIF4E phosphorylation during the activation of cell growth. Biochem Soc Trans. 1997;25:503-509. (Pubitemid 27260860)
20. Grethe S, Ares MP, Andersson T, Porn-Ares MI. p38 MAPK mediates TNF-induced apoptosis in endothelial cells via phosphorylation and downregulation of Bcl-x(L). Exp Cell Res. 2004;298:632-642. (Pubitemid 38950878)
21. Elia A, Constantinou C, Clemens MJ. Effects of protein phosphorylation on ubiquitination and stability of the translational inhibitor protein 4E-BP1. Oncogene. 2008;27:811-822. (Pubitemid 351186316)
22. Franklin CC, Kraft AS. Conditional expression of the mitogen-activated protein kinase (MAPK) phosphatase MKP-1 preferentially inhibits p38 MAPK and stress-activated protein kinase in U937 cells. J Biol Chem. 1997;272:16917- 16923. (Pubitemid 27289792)
23. Sun H, Charles CH, Lau LF, Tonks NK. MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell. 1993;75:487-493. (Pubitemid 23335074)
24. Hu JH, Chen T, Zhuang ZH, Kong L, Yu MC, Liu Y, Zang JW, Ge BX. Feedback control of MKP-1 expression by p38. Cell Signal. 2007;19: 393-400. (Pubitemid 46017084)
25. Guan L, Song K, Pysz MA, Curry KJ, Hizli AA, Danielpour D, Black AR, Black JD. Protein kinase C-mediated down-regulation of cyclin D1 involves activation of the translational repressor 4E-BP1 via a phosphoinositide 3-kinase/Akt-independent, protein phosphatase 2A-dependent mechanism in intestinal epithelial cells. J Biol Chem. 2007;282: 14213-14225. (Pubitemid 47100475)
26. Boudreau RT, Conrad DM, Hoskin DW. Apoptosis induced by protein phosphatase 2A (PP2A) inhibition in T leukemia cells is negatively regulated by PP2A-associated p38 mitogen-activated protein kinase. Cell Signal. 2007;19:139-151. (Pubitemid 44883367)
27. Cornell TT, Hinkovska-Galcheva V, Sun L, Cai Q, Hershenson MB, Vanway S, Shanley TP. Ceramide-dependent PP2A regulation of TNFα-induced IL-8 production in respiratory epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2009;296:L849-L856.
28. Lee T, Kim SJ, Sumpio BE. Role of PP2A in the regulation of p38 MAPK activation in bovine aortic endothelial cells exposed to cyclic strain. J Cell Physiol. 2003;194:349-355. (Pubitemid 36176895)
29. Fan WJ, Van Vuuren D, Genade S, Lochner A. Kinases and phosphatases in ischaemic preconditioning: a re-evaluation. Basic Res Cardiol. 2010; 105:495-511.
30. Clemens MJ, Bushell M, Jeffrey IW, Pain VM, Morley SJ. Translation initiation factor modifications and the regulation of protein synthesis in apoptotic cells. Cell Death Differ. 2000;7:603-615. (Pubitemid 30456166)
31. Sonenberg N, Morgan MA, Merrick WC, Shatkin AJ. A polypeptide in eukaryotic initiation factors that crosslinks specifically to the 5′-terminal cap in mRNA. Proc Natl Acad Sci USA. 1978;75:4843-4847. (Pubitemid 9048631)
32. Herbert TP, Tee AR, Proud CG. The extracellular signal-regulated kinase pathway regulates the phosphorylation of 4E-BP1 at multiple sites. J Biol Chem. 2002;277:11591-11596. (Pubitemid 34952931)
33. Clemens MJ. Translational regulation in cell stress and apoptosis. Roles of the eIF4E binding proteins. J Cell Mol Med. 2001;5:221-239.
34. Jeffrey IW, Elia A, Bornes S, Tilleray VJ, Gengatharan K, Clemens MJ. Interferon-α induces sensitization of cells to inhibition of protein synthesis by tumour necrosis factor-related apoptosis-inducing ligand. FEBS J. 2006;273:3698-3708. (Pubitemid 44166651)
35. Gingras AC, Kennedy SG, O'Leary MA, Sonenberg N, Hay N. 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes Dev. 1998;12:502-513. (Pubitemid 28101013)
36. Peterson RT, Desai BN, Hardwick JS, Schreiber SL. Protein phosphatase 2A interacts with the 70-kDa S6 kinase and is activated by inhibition of FKBP12-rapamycin-associated protein. Proc Natl Acad Sci USA. 1999; 96:4438-4442. (Pubitemid 29190354)
37. Meier R, Rouse J, Cuenda A, Nebreda AR, Cohen P. Cellular stresses and cytokines activate multiple mitogen-activated-protein kinase kinase homologues in PC12 and KB cells. Eur J Biochem. 1996;236:796-805. (Pubitemid 26112909)
38. Tilly BC, Gaestel M, Engel K, Edixhoven MJ, de Jonge HR. Hypoosmotic cell swelling activates the p38 MAP kinase signalling cascade. FEBS Lett. 1996;395:133-136. (Pubitemid 26356170)
39. Walsh D, Mohr I. Phosphorylation of eIF4E by Mnk-1 enhances HSV-1 translation and replication in quiescent cells. Genes Dev. 2004;18: 660-672. (Pubitemid 38489934)
40. Bochkov VN, Oskolkova OV, Birukov KG, Levonen AL, Binder CJ, Stockl J. Generation and biological activities of oxidized phospholipids. Antioxid Redox Signal. 12:1009-1059.
41. Berliner JA, Gharavi NM. Endothelial cell regulation by phospholipid oxidation products. Free Radic Biol Med. 2008;45:119-123.