2,282
Views
12
CrossRef citations to date
0
Altmetric
Research Paper

Regulation of gene expression by translation factor eIF5A: Hypusine-modified eIF5A enhances nonsense-mediated mRNA decay in human cells

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Article: e1366294 | Received 13 Jun 2017, Accepted 07 Aug 2017, Published online: 28 Sep 2017

References

  • Hershey JW, Sonenberg N, Mathews MB. Principles of translational control: an overview. Cold Spring Harb Perspect Biol. 2012;4:1-10. doi:10.1101/cshperspect.a011528. PMID:23209153
  • Shoemaker CJ, Green R. Translation drives mRNA quality control. Nat Struct Mol Biol. 2012;19:594-601. doi:10.1038/nsmb.2301. PMID:22664987
  • Celik A, Kervestin S, Jacobson A. NMD: At the crossroads between translation termination and ribosome recycling. Biochimie. 2015;114:2-9. doi:10.1016/j.biochi.2014.10.027. PMID:25446649
  • Lykke-Andersen S, Jensen TH. Nonsense-mediated mRNA decay: an intricate machinery that shapes transcriptomes. Nat Rev Mol Cell Biol. 2015;16:665-677. doi:10.1038/nrm4063. PMID:26397022
  • Popp MW, Maquat LE. Organizing principles of mammalian nonsense-mediatedmRNA decay. Annu Rev Genet. 2013;47:139-165. doi:10.1146/annurev-genet-111212-133424. PMID:24274751
  • Brogna S, McLeod T, Petric M. The meaning of NMD: translate or perish. Trends Genet. 2016;32:395-407. doi:10.1016/j.tig.2016.04.007. PMID:27185236
  • Fatscher T, Boehm V, Gehring NH. Mechanism, factors, and physiological role of nonsense-mediated mRNA decay. Cell Mol Life Sci. 2015;72:4523-4544. doi:10.1007/s00018-015-2017-9. PMID:26283621
  • Smith JE, Baker KE. Nonsense-mediated RNA decay–a switch and dial for regulating gene expression. Bioessays. 2015;37:612-623. doi:10.1002/bies.201500007. PMID:25820233
  • Hamid FM, Makeyev EV. Emerging functions of alternative splicing coupled with nonsense-mediated decay. Biochem Soc Trans. 2014;42:1168-1173. doi:10.1042/BST20140066. PMID:25110020
  • Sibley CR. Regulation of gene expression through production of unstable mRNA isoforms. Biochem Soc Trans. 2014;42:1196-1205. doi:10.1042/BST20140102. PMID:25110025
  • Lewis BP, Green RE, Brenner SE. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc Natl Acad Sci U S A. 2003;100:189-192. doi:10.1073/pnas.0136770100. PMID:12502788
  • Mitrovich QM, Anderson P. Unproductively spliced ribosomal protein mRNAs are natural targets of mRNA surveillance in C. elegans. Genes Dev. 2000;14:2173-2184
  • Holbrook JA, Neu-Yilik G, Hentze MW, Kulozik AE. Nonsense-mediated decay approaches the clinic. Nat Genet. 2004;36:801-808. doi:10.1038/ng1403. PMID:15284851
  • Lejeune F, Maquat LE. Mechanistic links between nonsense-mediated mRNA decay and pre-mRNA splicing in mammalian cells.Curr Opin Cell Biol. 2005;17:309-315. doi:10.1016/j.ceb.2005.03.002. PMID:15901502
  • Miller JN, Pearce DA. Nonsense-mediated decay in genetic disease: friend or foe? Mutat Res Rev Mutat Res. 2014;762:52-64. doi:10.1016/j.mrrev.2014.05.001. PMID:25485595
  • Frischmeyer PA, Dietz HC. Nonsense-mediated mRNA decay in health and disease. Hum Mol Genet. 1999;8:1893-1900. PMID:10469842
  • Mort M, Ivanov D, Cooper DN, Chuzhanova NA. A meta-analysis of nonsense mutations causing human genetic disease. Hum Mutat. 2008;29:1037-1047. doi:10.1002/humu.20763. PMID:18454449
  • Keeling KM, Xue X, Gunn G, Bedwell DM. Therapeutics based on stop codon readthrough. Annu Rev Genomics Hum Genet. 2014;15:371-394. doi:10.1146/annurev-genom-091212-153527. PMID:24773318
  • Schweingruber C, Rufener SC, Zund D, Yamashita A, Muhlemann O. Nonsense-mediated mRNA decay – mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim Biophys Acta. 2013;1829:612-623. doi:10.1016/j.bbagrm.2013.02.005. PMID:23435113
  • Hurt JA, Robertson AD, Burge CB. Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res. 2013;23:1636-1650. doi:10.1101/gr.157354.113. PMID:23766421
  • Nagy E, Maquat LE. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem Sci. 1998;23:198-199. PMID:9644970
  • Mathews MB, Hershey JW. The translation factor eIF5A and human cancer. Biochim Biophys Acta. 2015;1849:836-844. doi:10.1016/j.bbagrm.2015.05.002. PMID:25979826
  • Dever TE, Gutierrez E, Shin BS. The hypusine-containing translation factor eIF5A. Crit Rev Biochem Mol Biol. 2014;49:413-425. doi:10.3109/10409238.2014.939608. PMID:25029904
  • Kemper WM, Berry KW, Merrick WC. Purification and properties of rabbit reticulocyte protein synthesis initiation factors M2Balpha and M2Bbeta. J Biol Chem. 1976;251:5551-5557. PMID:965377
  • Benne R, Brown-Luedi ML, Hershey JW. Purification and characterization of protein synthesis initiation factors eIF-1, eIF-4C, eIF-4D, and eIF-5 from rabbit reticulocytes. J Biol Chem. 1978;253:3070-3077. PMID:641055
  • Saini P, Eyler DE, Green R, Dever TE. Hypusine-containing protein eIF5A promotes translation elongation. Nature. 2009;459:118-121. doi:10.1038/nature08034. PMID:19424157
  • Gutierrez E, Shin BS, Woolstenhulme CJ, Kim JR, Saini P, Buskirk AR, Dever TE, et al. eIF5A promotes translation of polyproline motifs. Mol Cell. 2013;51:35-45. doi:10.1016/j.molcel.2013.04.021. PMID:23727016
  • Schuller AP, Wu CC, Dever TE, Buskirk AR, Green R. eIF5A Functions Globally in Translation Elongation and Termination. Mol Cell. 2017;66:194-205 e195. doi:10.1016/j.molcel.2017.03.003. PMID:28392174
  • Pelechano V, Alepuz P. eIF5A facilitates translation termination globally and promotes the elongation of many non polyproline-specific tripeptide sequences. Nucleic Acids Research. 2017;45:7326-7338. doi:10.1093/nar/gkx479
  • Kang HA, Hershey JW. Effect of initiation factor eIF-5A depletion on protein synthesis and proliferation of Saccharomyces cerevisiae. J Biol Chem. 1994;269:3934-3940. PMID:8307948
  • Schrader R, Young C, Kozian D, Hoffmann R, Lottspeich F. Temperature-sensitive eIF5A mutant accumulates transcripts targeted to the nonsense-mediated decay pathway. J Biol Chem. 2006;281:35336-35346. PMID:16987817
  • Hanauske-Abel HM, Slowinska B, Zagulska S, Wilson RC, Staiano-Coico L, Hanauske AR, McCaffrey T, Szabo P.. Detection of a sub-set of polysomal mRNAs associated with modulation of hypusine formation at the G1-S boundary. Proposal of a role for eIF-5A in onset of DNA replication. FEBS Lett. 1995;366:92-98. PMID:7789538
  • Memin E, Hoque M, Jain MR, Heller DS, Li H, Cracchiolo B, Hanauske-Abel HM, Pe'ery T, Mathews MB. Blocking eIF5A modification in cervical cancer cells alters the expression of cancer-related genes and suppresses cell proliferation. Cancer Res. 2014;74:552-562. doi:10.1158/0008-5472.CAN-13-0474. PMID:24220243
  • Fujimura K, Choi S, Wyse M, Strnadel J, Wright T, Klemke R. Eukaryotic translation initiation Factor 5A (EIF5A) regulates pancreatic cancer metastasis by modulating RhoA and Rho-associated Kinase (ROCK) protein expression Levels. J Biol Chem. 2015;290:29907-29919. doi:10.1074/jbc.M115.687418. PMID:26483550
  • Mandal A, Mandal S, Park MH. Global quantitative proteomics reveal up-regulation of endoplasmic reticulum stress response proteins upon depletion of eIF5A in HeLa cells. Sci Rep. 2016;6:25795. doi:10.1038/srep25795. PMID:27180817
  • Taylor CA, Sun Z, Cliche DO, Ming H, Eshaque B, Jin S, Hopkins MT, Thai B, Thompson JE. Eukaryotic translation initiation factor 5A induces apoptosis in colon cancer cells and associates with the nucleus in response to tumour necrosis factor alpha signalling. Exp Cell Res. 2007;313:437-449. PMID:17187778
  • Luchessi AD, Cambiaghi TD, Hirabara SM, Lambertucci RH, Silveira LR, Baptista IL, Moriscot AS, Costa-Neto CM, Curi R. Involvement of eukaryotic translation initiation factor 5A (eIF5A) in skeletal muscle stem cell differentiation. J Cell Physiol. 2009;218:480-489. doi:10.1002/jcp.21619. PMID:19006180
  • Hanauske-Abel HM, Park MH, Hanauske AR, Popowicz AM, Lalande M, Folk JE. Inhibition of the G1-S transition of the cell cycle by inhibitors of deoxyhypusine hydroxylation. Biochim Biophys Acta. 1994;1221:115-124. PMID:8148388
  • Hofmann W, Reichart B, Ewald A, Müller E, Schmitt I, Stauber RH, Lottspeich F, Jockusch BM, Scheer U, Hauber J, et al. Cofactor requirements for nuclear export of Rev response element (RRE)- and constitutive transport element (CTE)-containing retroviral RNAs. an unexpected role for actin. J Cell Biol. 2001;152:895-910.
  • Hoque M, Hanauske-Abel HM, Palumbo P, Saxena D, D'Alliessi Gandolfi D, Park MH, Pe'ery T, Mathews MB. Inhibition of HIV-1 gene expression by Ciclopirox and Deferiprone, drugs that prevent hypusination of eukaryotic initiation factor 5A. Retrovirology. 2009;6:90. doi:10.1186/1742-4690-6-90. PMID:19825182
  • Li Y, Fu L, Li JB, Qin Y, Zeng TT, Zhou J, Zeng ZL, Chen J, Cao TT, Ban X, et al. Increased expression of EIF5A2, via hypoxia or gene amplification, contributes to metastasis and angiogenesis of esophageal squamous cell carcinoma. Gastroenterology. 2014;146:1701-1713 e1709. doi:10.1053/j.gastro.2014.02.029. PMID:24561231
  • Hanauske-Abel HM, Saxena D, Palumbo PE, Hanauske AR, Luchessi AD, Cambiaghi TD, Hoque M, Spino M, D'Alliessi Gandolfi D, Heller DS, et al. Drug-induced reactivation of apoptosis abrogates HIV-1 infection. PloS One. 2013;8:e74414. doi:10.1371/journal.pone.0074414. PMID:24086341
  • Olsen ME, Filone CM, Rozelle D, Mire CE, Agans KN, Hensley L, Connor JH. Polyamines and hypusination are required for ebolavirus gene expression and replication. MBio. 2016;7(4):e00882-16. doi:10.1128/mBio.00882-16
  • Bevec D, Jaksche H, Oft M, Wöhl T, Himmelspach M, Pacher A, Schebesta M, Koettnitz K, Dobrovnik M, Csonga R, et al. Inhibition of HIV-1 replication in lymphocytes by mutants of the Rev cofactor eIF-5A. Science. 1996;271:1858-1860. PMID:8596953
  • Zuk D, Jacobson A. A single amino acid substitution in yeast eIF-5A results in mRNA stabilization. EMBO J. 1998;17:2914-2925. doi:10.1093/emboj/17.10.2914. PMID:9582285
  • Valentini SR, Casolari JM, Oliveira CC, Silver PA, McBride AE. Genetic interactions of yeast eukaryotic translation initiation factor 5A (eIF5A) reveal connections to poly(A)-binding protein and protein kinase C signaling. Genetics. 2002;160:393-405. PMID:11861547
  • Rossi D, Galvão FC, Bellato HM, Boldrin PE, Andrews BJ, Valentini SR, Zanelli CF. eIF5A has a function in the cotranslational translocation of proteins into the ER. Amino Acids. 2014;46:645-653. doi:10.1007/s00726-013-1618-6. PMID:24306454
  • Zanelli CF, Valentini SR. Pkc1 acts through Zds1 and Gic1 to suppress growth and cell polarity defects of a yeast eIF5A mutant. Genetics. 2005;171:1571-1581. doi:10.1534/genetics.105.048082. PMID:16157662
  • Chatterjee I, Gross SR, Kinzy TG, Chen KY. Rapid depletion of mutant eukaryotic initiation factor 5A at restrictive temperature reveals connections to actin cytoskeleton and cell cycle progression. Mol Genet Genomics. 2006;275:264-276. PMID:16408210
  • Park MH, Cooper HL, Folk JE. Identification of hypusine, an unusual amino acid, in a protein from human lymphocytes and of spermidine as its biosynthetic precursor. Proc Natl Acad Sci U S A. 1981;78:2869-2873. PMID:6789324
  • Cooper HL, Park MH, Folk JE, Safer B, Braverman R. Identification of the hypusine-containing protein hy+ as translation initiation factor eIF-4D. Proc Natl Acad Sci U S A. 1983;80:1854-1857. PMID:6403941
  • Park MH. The post-translational synthesis of a polyamine-derived amino acid, hypusine, in the eukaryotic translation initiation factor 5A (eIF5A). J Biochem. 2006;139:161-169. PMID:16452303
  • Andrus L, Szabo P, Grady RW, Hanauske AR, Huima-Byron T, Slowinska B, Zagulska S, Hanauske-Abel HM. Antiretroviral effects of deoxyhypusyl hydroxylase inhibitors: a hypusine-dependent host cell mechanism for replication of human immunodeficiency virus type 1 (HIV-1). Biochem Pharmacol. 1998;55:1807-1818. PMID:9714299
  • Saxena D, Spino M, Tricta F, Connelly J, Cracchiolo BM, Hanauske AR, D'Alliessi Gandolfi D, Mathews MB, Karn J, Holland B, et al. Drug-Based Lead Discovery: The Novel Ablative Antiretroviral Profile of Deferiprone in HIV-1-infected cells and in HIV-infected treatment-naive subjects of a double-blind, placebo-controlled, randomized exploratory trial. PloS One. 2016;11:e0154842. doi:10.1371/journal.pone.0154842. PMID:27191165
  • Groskreutz DJ, Sherf BA, Wood KV, Schenborn ET. Increased expression and convenience with the new pGL3 luciferase reporter vectors. Promega Notes Magazine 1995;50:2-6.
  • Sun X, Perlick HA, Dietz HC, Maquat LE. A mutated human homologue to yeast Upf1 protein has a dominant-negative effect on the decay of nonsense-containing mRNAs in mammalian cells. Proc Natl Acad Sci U S A. 1998;95:10009-10014. PMID:9707591
  • Woeller CF, Gaspari M, Isken O, Maquat LE. NMD resulting from encephalomyocarditis virus IRES-directed translation initiation seems to be restricted to CBP80/20-bound mRNA. EMBO Rep. 2008;9:446-451. doi:10.1038/embor.2008.36. PMID:18369367
  • Duncan RF, Hershey JW. Changes in eIF-4D hypusine modification or abundance are not correlated with translational repression in HeLa cells. J Biol Chem. 1986;261:12903-12906. PMID:3091607
  • Wolff EC, Kang KR, Kim YS, Park MH. Posttranslational synthesis of hypusine: evolutionary progression and specificity of the hypusine modification. Amino Acids. 2007;33:341-350. PMID:17476569
  • Cuccurese M, Russo G, Russo A, Pietropaolo C. Alternative splicing and nonsense-mediated mRNA decay regulate mammalian ribosomal gene expression. Nucleic Acids Research. 2005;33:5965-5977. doi:10.1093/nar/gki905. PMID:16254077
  • Rossbach O, Hung LH, Schreiner S, Grishina I, Heiner M, Hui J, Bindereif A. Auto- and cross-regulation of the hnRNP L proteins by alternative splicing. Mol Cell Biol. 2009;29:1442-1451. doi:10.1128/MCB.01689-08. PMID:19124611
  • Hyvonen MT, Uimari A, Keinänen TA, Heikkinen S, Pellinen R, Wahlfors T, Korhonen A, Närvänen A, Wahlfors J, Alhonen L, et al. Polyamine-regulated unproductive splicing and translation of spermidine/spermine N1-acetyltransferase. RNA. 2006;12:1569-1582. doi:10.1261/rna.39806. PMID:16809818
  • Hauer C, Sieber J, Schwarzl T, Hollerer I, Curk T, Alleaume AM, Hentze MW, Kulozik A. Exon junction complexes show a distributional bias toward alternatively spliced mRNAs and against mRNAs coding for ribosomal proteins. Cell Rep. 2016;16:1588-1603. doi:10.1016/j.celrep.2016.06.096. PMID:27475226
  • Metze S, Herzog VA, Ruepp MD, Muhlemann O. Comparison of EJC-enhanced and EJC-independent NMD in human cells reveals two partially redundant degradation pathways. RNA. 2013;19:1432-1448. doi:10.1261/rna.038893.113. PMID:23962664
  • Iadevaia V, Caldarola S, Tino E, Amaldi F, Loreni F. All translation elongation factors and the e, f, and h subunits of translation initiation factor 3 are encoded by 5′-terminal oligopyrimidine (TOP) mRNAs. RNA. 2008;14:1730-1736. doi:10.1261/rna.1037108. PMID:18658124
  • Meyuhas O, Kahan T. The race to decipher the top secrets of TOP mRNAs. Biochim Biophys Acta. 2015;1849:801-811. doi:10.1016/j.bbagrm.2014.08.015. PMID:25234618
  • Mandal A, Mandal S, Park MH. Genome-wide analyses and functional classification of proline repeat-rich proteins: potential role of eIF5A in eukaryotic evolution. PloS One. 2014;9:e111800. doi:10.1371/journal.pone.0111800. PMID:25364902
  • Hershey JW. Expression of initiation factor genes in mammalian cells. Biochimie. 1994;76:847-852. PMID:7880901
  • Lipowsky G, Bischoff FR, Schwarzmaier P, Kraft R, Kostka S, Hartmann E, Kutay U, Görlich D. Exportin 4: a mediator of a novel nuclear export pathway in higher eukaryotes. Embo J. 2000;19:4362-4371. PMID:10944119
  • Xu A, Jao DL, Chen KY. Identification of mRNA that binds to eukaryotic initiation factor 5A by affinity co-purification and differential display. Biochem J. 2004;384:585-590. PMID:15303967
  • Xu A, Chen KY. Hypusine is required for a sequence-specific interaction of eukaryotic initiation factor 5A with postsystematic evolution of ligands by exponential enrichment RNA. J Biol Chem. 2001;276:2555-2561. doi:10.1074/jbc.M008982200. PMID:11060315
  • Shi XP, Yin KC, Waxman L. Effects of inhibitors of RNA and protein synthesis on the subcellular distribution of the eukaryotic translation initiation factor, eIF-5A, and the HIV-1 rev protein. Biol Signals. 1997;6:143-149. PMID:9285097
  • Melnikov S, Mailliot J, Shin BS, Rigger L, Yusupova G, Micura R, Dever TE, Yusupov M Crystal structure of hypusine-containing translation factor eIF5A bound to a rotated eukaryotic ribosome. Journal of Molecular Biology. 2016;428:3570-3576. doi:10.1016/j.jmb.2016.05.011. PMID:27196944
  • Sievert H, Venz S, Platas-Barradas O, Dhople VM, Schaletzky M, Nagel CH, Braig M, Preukschas M, Pällmann N, Bokemeyer C. Protein-protein-interaction Network Organization of the hypusine modification system. Mol Cell Proteomics. 2012;11:1289-1305. doi:10.1074/mcp.M112.019059. PMID:22888148
  • Menon B, Gulappa T, Menon KM. Eukaryotic initiation factor 5A plays an essential role in luteinizing hormone receptor regulation. Mol Endocrinol. 2014;28:1796-1806. doi:10.1210/me.2014-1132. PMID:25216047
  • Gulappa T, Menon B, Menon KM. Hypusination of eukaryotic initiation factor 5A via cAMP-PKA-ERK1/2 pathway is required for ligand-induced downregulation of LH receptor mRNA expression in the ovary. Mol Cell Endocrinol. 2015;413:90-95. doi:10.1016/j.mce.2015.06.014. PMID:26116232
  • Minden MD, Hogge DE, Weir SJ, Kasper J, Webster DA, Patton L, Jitkova Y, Hurren R, Gronda M, Goard CA, et al. Oral ciclopirox olamine displays biological activity in a phase I study in patients with advanced hematologic malignancies. Am J Hematol. 2014;89:363-368. doi:10.1002/ajh.23640. PMID:24273151
  • Gonzalez-Hilarion S, Beghyn T, Jia J, Debreuck N, Berte G, Mamchaoui K, Mouly V, Gruenert DC, Déprez B, Lejeune F. Rescue of nonsense mutations by amlexanox in human cells. Orphanet J Rare Dis. 2012;7:58. doi:10.1186/1750-1172-7-58. PMID:22938201
  • Homan KT, Wu E, Cannavo A, Koch WJ, Tesmer JJ. Identification and characterization of amlexanox as a G protein-coupled receptor kinase 5 inhibitor. Molecules. 2014;19:16937-16949. doi:10.3390/molecules191016937. PMID:25340299
  • Hoque M, Ji Z, Zheng D, Luo W, Li W, You B, Park JY, Yehia G, Tian B. Analysis of alternative cleavage and polyadenylation by 3′ region extraction and deep sequencing. Nat Methods. 2013;10:133-139. doi:10.1038/nmeth.2288. PMID:23241633
  • Anders S, Pyl PT, Huber W. HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166-169. doi:10.1093/bioinformatics/btu638. PMID:25260700
  • Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357-359. doi:10.1038/nmeth.1923. PMID:22388286
  • Katz Y, Wang ET, Airoldi EM, Burge CB. Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nat Methods. 2010;7:1009-1015. doi:10.1038/nmeth.1528. PMID:21057496

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.