1,150
Views
5
CrossRef citations to date
0
Altmetric
Research Paper

Induction of cap-independent BiP (hsp-3) and Bcl-2 (ced-9) translation in response to eIF4G (IFG-1) depletion in C. elegans

, , , &
Article: e28935 | Received 10 Jan 2014, Accepted 16 Apr 2014, Published online: 29 Apr 2014

References

  • Kimble J, Crittenden SL. Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu Rev Cell Dev Biol 2007; 23:405 - 33; http://dx.doi.org/10.1146/annurev.cellbio.23.090506.123326; PMID: 17506698
  • Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 1999; 126:1011 - 22; PMID: 9927601
  • Imataka H, Gradi A, Sonenberg N. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J 1998; 17:7480 - 9; http://dx.doi.org/10.1093/emboj/17.24.7480; PMID: 9857202
  • Lamphear BJ, Kirchweger R, Skern T, Rhoads RE. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. Implications for cap-dependent and cap-independent translational initiation. J Biol Chem 1995; 270:21975 - 83; http://dx.doi.org/10.1074/jbc.270.37.21975; PMID: 7665619
  • Gradi A, Imataka H, Svitkin YV, Rom E, Raught B, Morino S, Sonenberg N. A novel functional human eukaryotic translation initiation factor 4G. Mol Cell Biol 1998; 18:334 - 42; PMID: 9418880
  • Imataka H, Olsen HS, Sonenberg N. A new translational regulator with homology to eukaryotic translation initiation factor 4G. EMBO J 1997; 16:817 - 25; http://dx.doi.org/10.1093/emboj/16.4.817; PMID: 9049310
  • Morino S, Imataka H, Svitkin YV, Pestova TV, Sonenberg N. Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region. Mol Cell Biol 2000; 20:468 - 77; http://dx.doi.org/10.1128/MCB.20.2.468-477.2000; PMID: 10611225
  • Keiper BD, Gan W, Rhoads RE. Protein synthesis initiation factor 4G. Int J Biochem Cell Biol 1999; 31:37 - 41; http://dx.doi.org/10.1016/S1357-2725(98)00130-7; PMID: 10216942
  • Bushell M, McKendrick L, Jänicke RU, Clemens MJ, Morley SJ. Caspase-3 is necessary and sufficient for cleavage of protein synthesis eukaryotic initiation factor 4G during apoptosis. FEBS Lett 1999; 451:332 - 6; http://dx.doi.org/10.1016/S0014-5793(99)00614-6; PMID: 10371215
  • Pestova TV, Shatsky IN, Hellen CU. Functional dissection of eukaryotic initiation factor 4F: the 4A subunit and the central domain of the 4G subunit are sufficient to mediate internal entry of 43S preinitiation complexes. Mol Cell Biol 1996; 16:6870 - 8; PMID: 8943342
  • Marissen WE, Lloyd RE. Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol Cell Biol 1998; 18:7565 - 74; PMID: 9819442
  • Henis-Korenblit S, Strumpf NL, Goldstaub D, Kimchi A. A novel form of DAP5 protein accumulates in apoptotic cells as a result of caspase cleavage and internal ribosome entry site-mediated translation. Mol Cell Biol 2000; 20:496 - 506; http://dx.doi.org/10.1128/MCB.20.2.496-506.2000; PMID: 10611228
  • Marissen WE, Gradi A, Sonenberg N, Lloyd RE. Cleavage of eukaryotic translation initiation factor 4GII correlates with translation inhibition during apoptosis. Cell Death Differ 2000; 7:1234 - 43; http://dx.doi.org/10.1038/sj.cdd.4400750; PMID: 11175261
  • Nevins TA, Harder ZM, Korneluk RG, Holcík M. Distinct regulation of internal ribosome entry site-mediated translation following cellular stress is mediated by apoptotic fragments of eIF4G translation initiation factor family members eIF4GI and p97/DAP5/NAT1. J Biol Chem 2003; 278:3572 - 9; http://dx.doi.org/10.1074/jbc.M206781200; PMID: 12458215
  • Contreras V, Friday AJ, Morrison JK, Hao E, Keiper BD. Cap-independent translation promotes C. elegans germ cell apoptosis through Apaf-1/CED-4 in a caspase-dependent mechanism. PLoS One 2011; 6:e24444; http://dx.doi.org/10.1371/journal.pone.0024444; PMID: 21909434
  • Contreras V, Richardson MA, Hao E, Keiper BD. Depletion of the cap-associated isoform of translation factor eIF4G induces germline apoptosis in C. elegans. Cell Death Differ 2008; 15:1232 - 42; http://dx.doi.org/10.1038/cdd.2008.46; PMID: 18451872
  • De Benedetti A, Graff JR. eIF-4E expression and its role in malignancies and metastases. Oncogene 2004; 23:3189 - 99; http://dx.doi.org/10.1038/sj.onc.1207545; PMID: 15094768
  • Holcik M, Sonenberg N. Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 2005; 6:318 - 27; http://dx.doi.org/10.1038/nrm1618; PMID: 15803138
  • Yang Q, Sarnow P. Location of the internal ribosome entry site in the 5′ non-coding region of the immunoglobulin heavy-chain binding protein (BiP) mRNA: evidence for specific RNA-protein interactions. Nucleic Acids Res 1997; 25:2800 - 7; http://dx.doi.org/10.1093/nar/25.14.2800; PMID: 9207027
  • Lee AS. The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 2005; 35:373 - 81; http://dx.doi.org/10.1016/j.ymeth.2004.10.010; PMID: 15804610
  • Sherrill KW, Byrd MP, Van Eden ME, Lloyd RE. BCL-2 translation is mediated via internal ribosome entry during cell stress. J Biol Chem 2004; 279:29066 - 74; http://dx.doi.org/10.1074/jbc.M402727200; PMID: 15123638
  • Coldwell MJ, Mitchell SA, Stoneley M, MacFarlane M, Willis AE. Initiation of Apaf-1 translation by internal ribosome entry. Oncogene 2000; 19:899 - 905; http://dx.doi.org/10.1038/sj.onc.1203407; PMID: 10702798
  • Zhou Z, Hartwieg E, Horvitz HR. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 2001; 104:43 - 56; http://dx.doi.org/10.1016/S0092-8674(01)00190-8; PMID: 11163239
  • Hengartner MO, Ellis RE, Horvitz HR. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 1992; 356:494 - 9; http://dx.doi.org/10.1038/356494a0; PMID: 1560823
  • Chinnaiyan AM, O’Rourke K, Lane BR, Dixit VM. Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death. Science 1997; 275:1122 - 6; http://dx.doi.org/10.1126/science.275.5303.1122; PMID: 9027312
  • Pourkarimi E, Greiss S, Gartner A. Evidence that CED-9/Bcl2 and CED-4/Apaf-1 localization is not consistent with the current model for C. elegans apoptosis induction. Cell Death Differ 2012; 19:406 - 15; http://dx.doi.org/10.1038/cdd.2011.104; PMID: 21886181
  • Li D, Wang M. Construction of a bicistronic vector for the co-expression of two genes in Caenorhabditis elegans using a newly identified IRES. Biotechniques 2012; 52:173 - 6; PMID: 22401550
  • Cho S, Park SM, Kim TD, Kim JH, Kim KT, Jang SK. BiP internal ribosomal entry site activity is controlled by heat-induced interaction of NSAP1. Mol Cell Biol 2007; 27:368 - 83; http://dx.doi.org/10.1128/MCB.00814-06; PMID: 17074807
  • Heschl MF, Baillie DL. The HSP70 multigene family of Caenorhabditis elegans. Comp Biochem Physiol B 1990; 96:633 - 7; http://dx.doi.org/10.1016/0305-0491(90)90206-9; PMID: 2225768
  • Heschl MF, Baillie DL. Characterization of the hsp70 multigene family of Caenorhabditis elegans. DNA 1989; 8:233 - 43; http://dx.doi.org/10.1089/dna.1.1989.8.233; PMID: 2766926
  • Sherrill KW, Byrd MP, Van Eden ME, Lloyd RE. BCL-2 translation is mediated via internal ribosome entry during cell stress. J Biol Chem 2004; 279:29066 - 74; http://dx.doi.org/10.1074/jbc.M402727200; PMID: 15123638
  • Galvin BD, Denning DP, Horvitz HR. SPK-1, an SR protein kinase, inhibits programmed cell death in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2011; 108:1998 - 2003; http://dx.doi.org/10.1073/pnas.1018805108; PMID: 21245325
  • Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell 2007; 129:465 - 72; http://dx.doi.org/10.1016/j.cell.2007.04.019; PMID: 17482542
  • Lang KJ, Kappel A, Goodall GJ. Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol Biol Cell 2002; 13:1792 - 801; http://dx.doi.org/10.1091/mbc.02-02-0017; PMID: 12006670
  • Weingarten-Gabbay S, Khan D, Liberman N, Yoffe Y, Bialik S, Das S, Oren M, Kimchi A. The translation initiation factor DAP5 promotes IRES-driven translation of p53 mRNA. Oncogene 2013; PMID: 23318444
  • Gilbert WV. Alternative ways to think about cellular internal ribosome entry. J Biol Chem 2010; 285:29033 - 8; http://dx.doi.org/10.1074/jbc.R110.150532; PMID: 20576611
  • Malys N, McCarthy JE. Translation initiation: variations in the mechanism can be anticipated. Cell Mol Life Sci 2011; 68:991 - 1003; http://dx.doi.org/10.1007/s00018-010-0588-z; PMID: 21076851
  • Komar AA, Mazumder B, Merrick WC. A new framework for understanding IRES-mediated translation. Gene 2012; 502:75 - 86; http://dx.doi.org/10.1016/j.gene.2012.04.039; PMID: 22555019
  • Keiper BD, Rhoads RE. Cap-independent translation initiation in Xenopus oocytes. Nucleic Acids Res 1997; 25:395 - 402; http://dx.doi.org/10.1093/nar/25.2.395; PMID: 9016570
  • Buchkovich NJ, Yu Y, Pierciey FJ Jr., Alwine JC. Human cytomegalovirus induces the endoplasmic reticulum chaperone BiP through increased transcription and activation of translation by using the BiP internal ribosome entry site. J Virol 2010; 84:11479 - 86; http://dx.doi.org/10.1128/JVI.01330-10; PMID: 20739513
  • Koong AC, Auger EA, Chen EY, Giaccia AJ. The regulation of GRP78 and messenger RNA levels by hypoxia is modulated by protein kinase C activators and inhibitors. Radiat Res 1994; 138:Suppl S60 - 3; http://dx.doi.org/10.2307/3578763; PMID: 8146329
  • WormBase. hsp-3. In: R. Durbin JS, L. Stein and P. Sternberg, ed. WormBase: C elegans online database, 2007.
  • Dinkova TD, Keiper BD, Korneeva NL, Aamodt EJ, Rhoads RE. Translation of a small subset of Caenorhabditis elegans mRNAs is dependent on a specific eukaryotic translation initiation factor 4E isoform. Mol Cell Biol 2005; 25:100 - 13; http://dx.doi.org/10.1128/MCB.25.1.100-113.2005; PMID: 15601834
  • Rhoads RE, Lamphear BJ. Cap-independent translation of heat shock messenger RNAs. Curr Top Microbiol Immunol 1995; 203:131 - 53; http://dx.doi.org/10.1007/978-3-642-79663-0_7; PMID: 7555088
  • Joshi-Barve S, De Benedetti A, Rhoads RE. Preferential translation of heat shock mRNAs in HeLa cells deficient in protein synthesis initiation factors eIF-4E and eIF-4 gamma. J Biol Chem 1992; 267:21038 - 43; PMID: 1400417
  • Schneider RJ. Cap-independent translation in adenovirus infected cells. Curr Top Microbiol Immunol 1995; 203:117 - 29; http://dx.doi.org/10.1007/978-3-642-79663-0_6; PMID: 7555087
  • Henderson MA, Cronland E, Dunkelbarger S, Contreras V, Strome S, Keiper BD. A germline-specific isoform of eIF4E (IFE-1) is required for efficient translation of stored mRNAs and maturation of both oocytes and sperm. J Cell Sci 2009; 122:1529 - 39; http://dx.doi.org/10.1242/jcs.046771; PMID: 19383718
  • Hengartner MO, Horvitz HR. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 1994; 76:665 - 76; http://dx.doi.org/10.1016/0092-8674(94)90506-1; PMID: 7907274
  • Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997; 90:405 - 13; http://dx.doi.org/10.1016/S0092-8674(00)80501-2; PMID: 9267021
  • Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995; 376:37 - 43; http://dx.doi.org/10.1038/376037a0; PMID: 7596430
  • Chinnaiyan AM, Chaudhary D, O’Rourke K, Koonin EV, Dixit VM. Role of CED-4 in the activation of CED-3. Nature 1997; 388:728 - 9; http://dx.doi.org/10.1038/41913; PMID: 9285582
  • Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997; 91:479 - 89; http://dx.doi.org/10.1016/S0092-8674(00)80434-1; PMID: 9390557
  • Bessereau JL, Wright A, Williams DC, Schuske K, Davis MW, Jorgensen EM. Mobilization of a Drosophila transposon in the Caenorhabditis elegans germ line. Nature 2001; 413:70 - 4; http://dx.doi.org/10.1038/35092567; PMID: 11544527
  • Granger L, Martin E, Ségalat L. Mos as a tool for genome-wide insertional mutagenesis in Caenorhabditis elegans: results of a pilot study. Nucleic Acids Res 2004; 32:e117; http://dx.doi.org/10.1093/nar/gnh111; PMID: 15310838
  • Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974; 77:71 - 94; PMID: 4366476