Inhibition of mRNA deadenylation and degradation by different types of cell stress (original) (raw)

Abstract

We have previously observed rapid and strong inhibition of mRNA deadenylation and degradation in response to UV-B light [Gowrishankar et al., Biol. Chem. 386 (2005), pp. 1287–1293]. Expression analysis using a microarray for inflammatory genes showed that UV-B light induces stabilization of all short-lived mRNAs assayed. Stabilization was observed in HeLa cells, as well as in the keratinocyte line HaCaT. It affected constitutively expressed mRNA species, as well as species induced by the inflammatory cytokine IL-1. Many of the latter encode proteins involved in inflammation, suggesting that stress-induced inhibition of mRNA deadenylation contributes to changes in inflammatory gene expression. Deadenylation and degradation of _tet-off_-expressed mRNAs were also inhibited upon exposure to H2O2. However, scavengers of reactive oxygen species did not interfere with UV-B-induced inhibition of degradation, arguing against the involvement of UV-induced H2O2 in these effects of UV-B light. Heat shock and hyperosmolarity also inhibited mRNA deadenylation and degradation, whereas γ-radiation did not. Thus, inhibition of mRNA deadenylation and degradation is a cellular response elicited by several but not all inducers of cell stress.

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Corresponding author holtmann.helmut@mh-hannover.de


References

Bakheet, T., Frevel, M., Williams, B.R., Greer, W., and Khabar, K.S. (2001). ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Res.29, 246–254.10.1093/nar/29.1.246Search in Google Scholar

Blattner, C., Kannouche, P., Litfin, M., Bender, K., Rahmsdorf, H.J., Angulo, J.F., and Herrlich, P. (2000). UV-Induced stabilization of c-fos and other short-lived mRNAs. Mol. Cell. Biol.20, 3616–3625.10.1128/MCB.20.10.3616-3625.2000Search in Google Scholar

Bollig, F., Winzen, R., Kracht, M., Ghebremedhin, B., Ritter, B., Wilhelm, A., Resch, K., and Holtmann, H. (2002). Evidence for general stabilization of mRNAs in response to UV light. Eur. J. Biochem.269, 5830–5839.10.1046/j.1432-1033.2002.03300.xSearch in Google Scholar

Chen, C.Y. and Shyu, A.B. (1995). AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci.20, 465–470.10.1016/S0968-0004(00)89102-1Search in Google Scholar

Gossen, M. and Bujard, H. (1992). Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA89, 5547–5551.10.1073/pnas.89.12.5547Search in Google Scholar PubMed PubMed Central

Gowrishankar, G., Winzen, R., Bollig, F., Ghebremedhin, B., Redich, N., Ritter, B., Resch, K., Kracht, M., and Holtmann, H. (2005). Inhibition of mRNA deadenylation and degradation by ultraviolet light. Biol. Chem.386, 1287–1293.10.1515/BC.2005.146Search in Google Scholar PubMed

Gross, S., Knebel, A., Tenev, T., Neininger, A., Gaestel, M., Herrlich, P., and Bohmer, F.D. (1999). Inactivation of protein-tyrosine phosphatases as mechanism of UV-induced signal transduction. J. Biol. Chem.274, 26378–26386.10.1074/jbc.274.37.26378Search in Google Scholar PubMed

Herrlich, P., Blattner, C., Knebel, A., Bender, K., and Rahmsdorf, H.J. (1997). Nuclear and non-nuclear targets of genotoxic agents in the induction of gene expression. Shared principles in yeast, rodents, man and plants. Biol. Chem.378, 1217–1229.Search in Google Scholar

Hoffmann, E., Dittrich-Breiholz, O., Holtmann, H., and Kracht, M. (2002). Multiple control of interleukin-8 gene expression. J. Leukoc. Biol.72, 847–855.10.1189/jlb.72.5.847Search in Google Scholar

Holzberg, D., Knight, C.G., Dittrich-Breiholz, O., Schneider, H., Dorrie, A., Hoffmann, E., Resch, K., and Kracht, M. (2003). Disruption of the c-JUN-JNK complex by a cell-permeable peptide containing the c-JUN delta domain induces apoptosis and affects a distinct set of interleukin-1-induced inflammatory genes. J. Biol. Chem.278, 40213–40223.10.1074/jbc.M304058200Search in Google Scholar PubMed

Lasa, M., Mahtani, K.R., Finch, A., Brewer, G., Saklatvala, J., and Clark, A.R. (2000). Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell. Biol.20, 4265–4274.10.1128/MCB.20.12.4265-4274.2000Search in Google Scholar PubMed PubMed Central

Parker, R. and Song, H. (2004). The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol.11, 121–127.10.1038/nsmb724Search in Google Scholar PubMed

Peus, D., Vasa, R.A., Meves, A., Pott, M., Beyerle, A., Squillace, K., and Pittelkow, M.R. (1998). H2O2 is an important mediator of UVB-induced EGF-receptor phosphorylation in cultured keratinocytes. J. Invest. Dermatol.110, 966–971.10.1046/j.1523-1747.1998.00210.xSearch in Google Scholar PubMed

Tyrrell, R.M. (1996). Activation of mammalian gene expression by the UV component of sunlight – from models to reality. Bioessays18, 139–148.10.1002/bies.950180210Search in Google Scholar PubMed

Wang, W., Furneaux, H., Cheng, H., Caldwell, M.C., Hutter, D., Liu, Y., Holbrook, N., and Gorospe, M. (2000). HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol.20, 760–769.10.1128/MCB.20.3.760-769.2000Search in Google Scholar PubMed PubMed Central

White, F.C., Benehacene, A., Scheele, J.S., and Kamps, M. (1997). VEGF mRNA is stabilized by ras and tyrosine kinase oncogenes, as well as by UV radiation – evidence for divergent stabilization pathways. Growth Factors14, 199–212.10.3109/08977199709021520Search in Google Scholar PubMed

Winzen, R., Kracht, M., Ritter, B., Wilhelm, A., Chen, C.Y., Shyu, A.B., Muller, M., Gaestel, M., Resch, K., and Holtmann, H. (1999). The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J.18, 4969–4980.10.1093/emboj/18.18.4969Search in Google Scholar PubMed PubMed Central

Published Online: 2006-03-17

Published in Print: 2006-03-01

©2006 by Walter de Gruyter Berlin New York