Reprogramming MRNA Translation During Stress

Overview

Journal Curr Opin Cell Biol

Publisher Elsevier

Specialty Cell Biology

Date 2008 Mar 22

PMID 18356035

Citations 113

Authors

Satoshi Yamasaki

Paul Anderson

Affiliations

Soon will be listed here.

Abstract

The survival of mammalian cells exposed to adverse environmental conditions requires a radical reprogramming of protein translation. Stress-activated kinases target components of the initiation machinery (e.g. eIF2alpha, eIF4E-BP, eIF4B, and ribosomal protein S6) to inhibit the translation of 'housekeeping' proteins and promote the translation of repair enzymes. Accumulating untranslated mRNA is concentrated at stress granules where it is sorted and triaged to sites of storage, reinitiation, or decay. At the same time, the translation of mRNAs encoding repair enzymes is selectively preserved by both internal ribosome entry site-dependent and -independent mechanisms. In combination, these stress-activated processes coordinately reprogram mRNA translation and decay in a way that conserves anabolic energy, preserves essential mRNAs, and promotes the repair of stress-induced molecular damage.

Citing Articles

The Steamer-like Element-1 Retrotransposon Antisense mRNA Harbors an Internal Ribosome Entry Site That Is Modulated by hnRNPK.

Fernandez-Garcia L, Ahumada-Marchant C, Lobos-Avila P, Brauer B, Bustos F, Arriagada G Viruses. 2024; 16(3).

PMID: 38543768 PMC: 10974842. DOI: 10.3390/v16030403.

Tailoring the stress response of human skin cells by substantially limiting the nuclear localization of angiogenin.

Culurciello R, Di Nardo I, Bosso A, Tortora F, Troisi R, Sica F Heliyon. 2024; 10(3):e24556.

PMID: 38317956 PMC: 10839879. DOI: 10.1016/j.heliyon.2024.e24556.

Seneca Valley virus 3C antagonizes host innate immune responses and programmed cell death.

Zhang X, Li Y, Huang H, Zhao C, Lei X, Zhao B Front Microbiol. 2023; 14:1235620.

PMID: 37869659 PMC: 10588452. DOI: 10.3389/fmicb.2023.1235620.

The role of m5C methyltransferases in cardiovascular diseases.

Wang Y, Tian Y, Li Y, Liu Y, Zhao Y, Chen L Front Cardiovasc Med. 2023; 10:1225014.

PMID: 37476573 PMC: 10354557. DOI: 10.3389/fcvm.2023.1225014.

MicroRNAs in Age-Related Proteostasis and Stress Responses.

Matai L, Slack F Noncoding RNA. 2023; 9(2).

PMID: 37104008 PMC: 10143298. DOI: 10.3390/ncrna9020026.

References

Scheper G, van der Knaap M, Proud C . Translation matters: protein synthesis defects in inherited disease. Nat Rev Genet. 2007; 8(9):711-23. DOI: 10.1038/nrg2142. View

Reiling J, Sabatini D . Stress and mTORture signaling. Oncogene. 2006; 25(48):6373-83. DOI: 10.1038/sj.onc.1209889. View

Keegan L, Gallo A, OConnell M . The many roles of an RNA editor. Nat Rev Genet. 2001; 2(11):869-78. DOI: 10.1038/35098584. View

Fernandez J, Yaman I, Huang C, Liu H, Lopez A, Komar A . Ribosome stalling regulates IRES-mediated translation in eukaryotes, a parallel to prokaryotic attenuation. Mol Cell. 2005; 17(3):405-16. DOI: 10.1016/j.molcel.2004.12.024. View

Hay N, Sonenberg N . Upstream and downstream of mTOR. Genes Dev. 2004; 18(16):1926-45. DOI: 10.1101/gad.1212704. View

Krishnamoorthy T, Pavitt G, Zhang F, Dever T, Hinnebusch A . Tight binding of the phosphorylated alpha subunit of initiation factor 2 (eIF2alpha) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol Cell Biol. 2001; 21(15):5018-30. PMC: 87228. DOI: 10.1128/MCB.21.15.5018-5030.2001. View

Rudra D, Warner J . What better measure than ribosome synthesis?. Genes Dev. 2004; 18(20):2431-6. DOI: 10.1101/gad.1256704. View

Tinton S, Schepens B, Bruynooghe Y, Beyaert R, Cornelis S . Regulation of the cell-cycle-dependent internal ribosome entry site of the PITSLRE protein kinase: roles of Unr (upstream of N-ras) protein and phosphorylated translation initiation factor eIF-2alpha. Biochem J. 2004; 385(Pt 1):155-63. PMC: 1134683. DOI: 10.1042/BJ20040963. View

Brostrom C, Brostrom M . Regulation of translational initiation during cellular responses to stress. Prog Nucleic Acid Res Mol Biol. 1997; 58:79-125. DOI: 10.1016/s0079-6603(08)60034-3. View

10.

McEwen E, Kedersha N, Song B, Scheuner D, Gilks N, Han A . Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J Biol Chem. 2005; 280(17):16925-33. DOI: 10.1074/jbc.M412882200. View

11.

Baird S, Turcotte M, Korneluk R, Holcik M . Searching for IRES. RNA. 2006; 12(10):1755-85. PMC: 1581980. DOI: 10.1261/rna.157806. View

12.

Moore M . From birth to death: the complex lives of eukaryotic mRNAs. Science. 2005; 309(5740):1514-8. DOI: 10.1126/science.1111443. View

13.

Scadden A . Inosine-containing dsRNA binds a stress-granule-like complex and downregulates gene expression in trans. Mol Cell. 2007; 28(3):491-500. PMC: 2075533. DOI: 10.1016/j.molcel.2007.09.005. View

14.

Samuel C . Antiviral actions of interferons. Clin Microbiol Rev. 2001; 14(4):778-809, table of contents. PMC: 89003. DOI: 10.1128/CMR.14.4.778-809.2001. View

15.

Wang Q, Miyakoda M, Yang W, Khillan J, Stachura D, Weiss M . Stress-induced apoptosis associated with null mutation of ADAR1 RNA editing deaminase gene. J Biol Chem. 2003; 279(6):4952-61. DOI: 10.1074/jbc.M310162200. View

16.

Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember L . Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell. 2004; 15(12):5383-98. PMC: 532018. DOI: 10.1091/mbc.e04-08-0715. View

17.

Kulshreshtha R, Ferracin M, E Wojcik S, Garzon R, Alder H, Agosto-Perez F . A microRNA signature of hypoxia. Mol Cell Biol. 2006; 27(5):1859-67. PMC: 1820461. DOI: 10.1128/MCB.01395-06. View

18.

Bhattacharyya S, Habermacher R, Martine U, Closs E, Filipowicz W . Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell. 2006; 125(6):1111-24. DOI: 10.1016/j.cell.2006.04.031. View

19.

Iwawaki T, Hosoda A, Okuda T, Kamigori Y, Kimata Y, Tsuru A . Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat Cell Biol. 2001; 3(2):158-64. DOI: 10.1038/35055065. View

20.

Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K . XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell. 2002; 107(7):881-91. DOI: 10.1016/s0092-8674(01)00611-0. View