Hyperoxia alters the expression and phosphorylation of multiple factors regulating translation initiation

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 288, Issue 3 32-3, 2005, Pages

  Shenberger, Jeffrey S ^a,d   Myers, Jennifer L ^a   Zimmer, Stephen G ^b   Powell, Richard J ^a   Barchowsky, Aaron ^c  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

Author keywords

Eukaryotic translation initiation factors; Lung; Protein synthesis; Stress granules

Indexed keywords

CAP BINDING PROTEIN; DNA; GUANOSINE TRIPHOSPHATE; INITIATION FACTOR 4E BINDING PROTEIN; ISOPROTEIN; LEUCINE; SERINE; THYMIDINE; TRANSFER RNA;

AMINO ACID METABOLISM; ARTICLE; BINDING AFFINITY; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DNA SYNTHESIS; HUMAN; HUMAN CELL; HYPEROXIA; LUNG FIBROBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; TRANSLATION INITIATION; TRANSLATION REGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CARRIER PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CYTOPLASMIC GRANULES; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTORS; FIBROBLASTS; HUMANS; HYPEROXIA; LEUCINE; LUNG; PEPTIDE ELONGATION FACTORS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITORS; STRESS, MECHANICAL; TIME FACTORS;

EID: 13644258997     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00127.2004     Document Type: Article

References (36)

1. Alirezaei M, Marin P, Nairn AC, Glowinski J, and Premont J. Inhibition of protein synthesis in cortical neurons during exposure to hydrogen peroxide. J Neurochem 76: 1080-1088, 2001.
2. Balin AK, Goodman BP, Rasmussen H, and Cristofalo VJ. The effect of oxygen tension on the growth and metabolism of WI-38 cells. J Cell Physiol 89: 235-249, 1976.
3. Berkel HJ, Turbat-Herrera EA, Shi R, and de Benedetti A. Expression of the translation initiation factor eIF4E in the polyp-cancer sequence in the colon. Cancer Epidemiol Biomarkers Prev 10: 663-666, 2001.
4. Browne GJ and Proud CG. Regulation of peptide-chain elongation in mammalian cells. Eur J Biochem 269: 5360-5368, 2002.
5. Cheema IR and Jones DL. TNF-α and cortisone impair peptide chain initiation by altering the availability of initiation factor EIF-4E. Front Biosci 8: S1051-S1055, 2003.
6. Duncan RF, Peterson H, Hagedorn CH, and Sevanian A. Oxidative stress increases eukaryotic initiation factor 4E phosphorylation in vascular cells. Biochem J 369: 213-225, 2003.
7. Gacad G and Massaro D. Hyperoxia: influence on lung mechanics and protein synthesis. J Clin Invest 52: 559-565, 1973.
8. Garcia L, Burda J, Hrehorovska M, Burda R, Martin ME, and Salinas M. Ischaemic preconditioning in the rat brain: effect on the activity of several initiation factors, Akt and extracellular signal-regulated protein kinase phosphorylation, and GRP78 and GADD34 expression. J Neurochem 88: 136-147, 2004.
9. Hayashi T, Saito A, Okuno S, Ferrand-Drake M, Dodd RL, Nishi T, Maier CM, Kinouchi H, and Chan PH. Oxidative damage to the endoplasmic reticulum is implicated in ischemic neuronal cell death. J Cereb Blood Flow Metab 23: 1117-1128, 2003.
10. Heesom KJ, Gampel A, Mellor H, and Denton RM. Cell cycle-dependent phosphorylation of the translational repressor eIF-4E binding protein-1 (4E-BP1). Curr Biol 11: 1374-1379, 2001.
11. Hinnebusch A. Mechanism and regulation of initiator methionyl-tRNA binding to ribosomes. In: Translational Control of Gene Expression, edited by Sonenberg NHJ, Hershey JWB, and Mathews MB. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 2000, p. 185-243.
12. Jornot L, Mirault ME, and Junod AF. Protein synthesis in hyperoxic endothelial cells: evidence for translational defect. J Appl Physiol 63: 457-464, 1987.
13. Kedersha N and Anderson P. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem Soc Trans 30: 963-969, 2002.
14. Kedersha N, Chen S, Gilks N, Li W, Miller U, Stahl J, and Anderson P. Evidence that ternary complex [eIF2-GTP-tRNA(i)(Met)]-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol Biol Cell 13: 195-210, 2002.
15. Kelly FJ. Effect of hyperoxic exposure on protein synthesis in the rat. Biochem J 249: 609-612, 1988.
16. Kim YM, Son K, Hong SJ, Green A, Chen JJ, Tzeng E, Hierholzer C, and Billiar TR. Inhibition of protein synthesis by nitric oxide correlates with cytostatic activity: nitric oxide induces phosphorylation of initiation factor eIF-2α. Mol Med 4: 179-190, 1998.
17. Kimball SR, Horetsky RL, Ron D, Jefferson LS, and Harding HP. Mammalian stress granules represent sites of accumulation of stalled translation initiation complexes. Am J Physiol Cell Physiol 284: C273-C284, 2003.
18. Knauf U, Tschopp C, and Gram H. Negative regulation of protein translation by mitogen-activated protein kinase-interacting kinases 1 and 2. Mol Cell Biol 21: 5500-5511, 2001.
19. Lachance PE, Miron M, Raught B, Sonenberg N, and Lasko P. Phosphorylation of eukaryotic translation initiation factor 4E is critical for growth. Mol Cell Biol 22: 1656-1663, 2002.
20. Lee PJ and Choi AM. Pathways of cell signaling in hyperoxia. Free Radic Biol Med 35: 341-350, 2003.
21. Long E, Capuco AV, and Zhao X. Cloning of bovine eukaryotic translation initiation factor 4E (eIF-4E) and its expression in the bovine mammary gland at different physiological stages. DNA Seq 12: 319-329, 2001.
22. Makhlouf AA, Namboodiri AM, and McDermott PJ. Transcriptional regulation of the rat eIF4E gene in cardiac muscle cells: the role of specific elements in the promoter region. Gene 267: 1-12, 2001.
23. McGrath SA. Induction of p21WAF/CIP1 during hyperoxia. Am J Respir Cell Mol Biol 18: 179-187, 1998.
24. Mothe-Satney I, Yang D, Fadden P, Haystead TA, and Lawrence JC Jr. Multiple mechanisms control phosphorylation of PHAS-I in five (S/T)P sites that govern translational repression. Mol Cell Biol 20: 3558-3567, 2000.
25. Murtha-Riel P, Davies MV, Scherer BJ, Choi SY, Hershey JW, and Kaufman RJ. Expression of a phosphorylation-resistant eukaryotic initiation factor 2 α-subunit mitigates heat shock inhibition of protein synthesis. J Biol Chem 268: 12946-12951, 1993.
26. Northway WH Jr, Petriceks R, and Shahinian L. Quantitative aspects of oxygen toxicity in the newborn: inhibition of lung DNA synthesis in the mouse. Pediatrics 50: 67-72, 1972.
27. Patel J, McLeod LE, Vries RG, Flynn A, Wang X, and Proud CG. Cellular stresses profoundly inhibit protein synthesis and modulate the states of phosphorylation of multiple translation factors. Eur J Biochem 269: 3076-3085, 2002.
28. Rancourt RC, Keng PC, Helt CE, and O'Reilly MA. The role of p21 (CIP1/WAF1) in growth of epithelial cells exposed to hyperoxia. Am J Physiol Lung Cell Mol Physiol 280: L617-L626, 2001.
29. Raught B and Gingras AC. eIF4E activity is regulated at multiple levels. Int J Biochem Cell Biol 31: 43-57, 1999.
30. Scheper GC, van Kollenburg B, Hu J, Luo Y, Goss DJ, and Proud CG. Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affinity for capped mRNA. J Biol Chem 277: 3303-3309, 2002.
31. Seki N, Takasu T, Mandai K, Nakata M, Saeki H, Heike Y, Takata I, Segawa Y, Hanafusa T, and Eguchi K. Expression of eukaryotic initiation factor 4E in atypical adenomatous hyperplasia and adenocarcinoma of the human peripheral lung. Clin Cancer Res 8: 3046-3053, 2002.
32. Shenberger JS, Adams MH, and Zimmer SG. Oxidant-induced hypertrophy of A549 cells is accompanied by alterations in eukaryotic translation initiation factor 4E and 4E-binding protein-1. Am J Respir Cell Mol Biol 27: 250-256, 2002.
33. Shenberger JS and Dixon PS. Oxygen induces S-phase growth arrest and increases p53 and p21(WAF1/CIP1) expression in human bronchial smooth muscle cells. Am J Respir Cell Mol Biol 21: 395-402, 1999.
34. Sonenberg N and Dever TE. Eukaryotic translation initiation factors and regulators. Curr Opin Struct Biol 13: 56-63, 2003.
35. Stancombe BB, Walsh WF, Derdak S, Dixon P, and Hensley D. Induction of human neonatal pulmonary fibroblast cytokines by hyperoxia and Ureaplasma urealyticum. Clin Infect Dis 17, Suppl 1: S154-S157, 1993.
36. Zuberek J, Wyslouch-Cieszynska A, Niedzwiecka A, Dadlez M, Stepinski J, Augustyniak W, Gingras AC, Zhang Z, Burley SK, Sonenberg N, Stolarski R, and Darzynkiewicz E. Phosphorylation of eIF4E attenuates its interaction with mRNA 5′ cap analogs by electrostatic repulsion: intein-mediated protein ligation strategy to obtain phosphorylated protein. RNA 9: 52-61, 2003.