The insulin receptor cellular IRES confers resistance to eIF4A inhibition

eLife

Volumn 2013, Issue 2, 2013, Pages

  Olson, Calla M ^a   Donovan, Marissa R ^a   Spellberg, Michael J ^a   Marr II, Michael T ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIPPURISTANOL; INITIATION FACTOR 4A; INITIATION FACTOR 4E; INSULIN RECEPTOR; PARAQUAT; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN INHIBITOR; SOMATOMEDIN C RECEPTOR; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG; 5' UNTRANSLATED REGION; CAPPED RNA;

5' UNTRANSLATED REGION; AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENE EXPRESSION; IMMUNOBLOTTING; INTERNAL RIBOSOME ENTRY SITE; MALE; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; RETICULOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSLATION REGULATION; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RIBOSOME; SEQUENCE HOMOLOGY;

5' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; DROSOPHILA; EUKARYOTIC INITIATION FACTOR-4A; MOLECULAR SEQUENCE DATA; RECEPTOR, INSULIN; RIBOSOMES; RNA CAPS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84880614734     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00542     Document Type: Article

References (47)

1. Bordeleau ME, Mori A, Oberer M, Lindqvist L, Chard LS, Higa T, et al. 2006. Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat Chem Biol 2:213-20. doi: 10.1038/nchembio776.
2. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, et al. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-68. doi: 10.1016/S0092-8674(00)80595-4.
3. Casas-Tinto S, Marr MT II, Andreu P, Puig O. 2007. Characterization of the Drosophila insulin receptor promoter. Biochim Biophys Acta 1769:236-43. doi: 10.1016/j.bbaexp.2007.03.003.
4. Cash AC, Andrews J. 2012. Fine scale analysis of gene expression in Drosophila melanogaster gonads reveals Programmed cell death 4 promotes the differentiation of female germline stem cells. BMC Dev Biol 12:4. doi: 10.1186/1471-213X-12-4.
5. Chang JH, Cho YH, Sohn SY, Choi JM, Kim A, Kim YC, et al. 2009. Crystal structure of the eIF4A-PDCD4 complex. Proc Natl Acad Sci USA 106:3148-53. doi: 10.1073/pnas.0808275106.
6. Dorrello NV, Peschiaroli A, Guardavaccaro D, Colburn NH, Sherman NE, Pagano M. 2006. S6K1- and betaTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science 314:467-71. doi: 10.1126/science.1130276.
7. Gebauer F, Corona DF, Preiss T, Becker PB, Hentze MW. 1999. Translational control of dosage compensation in Drosophila by Sex-lethal: cooperative silencing via the 5' and 3' UTRs of msl-2 mRNA is independent of the poly(A) tail. EMBO J 18:6146-54. doi: 10.1093/emboj/18.21.6146.
8. Gershman B, Puig O, Hang L, Peitzsch RM, Tatar M, Garofalo RS. 2007. High-resolution dynamics of the transcriptional response to nutrition in Drosophila: a key role for dFOXO. Physiol Genomics 29:24-34. doi: 10.1152/physiolgenomics.00061.2006.
9. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, Hoekstra MF, et al. 1999. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 13:1422-37. doi: 10.1101/gad.13.11.1422.
10. Giraud S, Greco A, Brink M, Diaz J-J, Delafontaine P. 2001. Translation initiation of the insulin-like growth factor I receptor mRNA is mediated by an internal ribosome entry site. J Biol Chem 276:5668-75. doi: 10.1074/jbc.M005928200.
11. Hernandez G, Vazquez-Pianzola P, Sierra JM, Rivera-Pomar R. 2004. Internal ribosome entry site drives cap-independent translation of reaper and heat shock protein 70 mRNAs in Drosophila embryos. RNA 10:1783-97. doi: 10.1261/rna.7154104.
12. Hu P, Geles KG, Paik JH, DePinho RA, Tjian R. 2008. Codependent activators direct myoblast-specific MyoD transcription. Dev Cell 15:534-46. doi: 10.1016/j.devcel.2008.08.018.
13. Iwasaki S, Kawamata T, Tomari Y. 2009. Drosophila argonaute1 and argonaute2 employ distinct mechanisms for translational repression. Mol Cell 34:58-67. doi: 10.1016/j.molcel.2009.02.010.
14. Junger MA, Rintelen F, Stocker H, Wasserman JD, Vegh M, Radimerski T, et al. 2003. The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2:20. doi: 10.1186/1475-4924-2-20.
15. Khodor YL, Rodriguez J, Abruzzi KC, Tang CH, Marr MT II, Rosbash M. 2011. Nascent-seq indicates widespread cotranscriptional pre-mRNA splicing in Drosophila. Genes Dev 25:2502-12. doi: 10.1101/gad.178962.111.
16. Kieft JS, Zhou K, Jubin R, Murray MG, Lau JY, Doudna JA. 1999. The hepatitis C virus internal ribosome entry site adopts an ion-dependent tertiary fold. J Mol Biol 292:513-29. doi: 10.1006/jmbi.1999.3095.
17. Lal A, Haynes SR, Gorospe M. 2005. Clean Western blot signals from immunoprecipitated samples. Mol Cell Probes 19:385-8. doi: 10.1016/j.mcp.2005.06.007.
18. Lindqvist L, Oberer M, Reibarkh M, Cencic R, Bordeleau ME, Vogt E, et al. 2008. Selective pharmacological targeting of a DEAD box RNA helicase. PLOS ONE 3:e1583. doi: 10.1371/journal.pone.0001583.
19. Ma XM, Blenis J. 2009. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10:307-18. doi: 10.1038/nrm2672.
20. Marr MT II, D'Alessio JA, Puig O, Tjian R. 2007. IRES-mediated functional coupling of transcription and translation amplifies insulin receptor feedback. Genes Dev 21:175-83. doi: 10.1101/gad.1506407.
21. Marr MT II, Isogai Y, Wright KJ, Tjian R. 2006. Coactivator cross-talk specifies transcriptional output. Genes Dev 20:1458-69. doi: 10.1101/gad.1418806.
22. Meng Z, Jackson NL, Choi H, King PH, Emanuel PD, Blume SW. 2008. Alterations in RNA-binding activities of IRES-regulatory proteins as a mechanism for physiological variability and pathological dysregulation of IGF-IR translational control in human breast tumor cells. J Cell Physiol 217:172-83. doi: 10.1002/jcp.21486.
23. Misra JR, Horner MA, Lam G, Thummel CS. 2011. Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes Dev 25:1796-806. doi: 10.1101/gad.17280911.
24. Nicol JW, Helt GA, Blanchard SG Jnr, Raja A, Loraine AE. 2009. The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25:2730-1. doi: 10.1093/bioinformatics/btp472.
25. Oldham S. 2011. Obesity and nutrient sensing TOR pathway in flies and vertebrates: functional conservation of genetic mechanisms. Trends Endocrinol Metab 22:45-52. doi: 10.1016/j.tem.2010.11.002.
26. Palamarchuk A, Efanov A, Maximov V, Aqeilan RI, Croce CM, Pekarsky Y. 2005. Akt phosphorylates and regulates Pdcd4 tumor suppressor protein. Cancer Res 65:11282-6. doi: 10.1158/0008-5472.CAN-05-3469.
27. Pestova TV, Shatsky IN, Fletcher SP, Jackson RJ, Hellen CU. 1998. A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev 12:67-83. doi: 10.1101/gad.12.1.67.
28. Puig O, Marr MT, Ruhf ML, Tjian R. 2003. Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev 17:2006-20. doi: 10.1101/gad.1098703.
29. Puig O, Tjian R. 2005. Transcriptional feedback control of insulin receptor by dFOXO/FOXO1. Genes Dev 19:2435-46. doi: 10.1101/gad.1340505.
30. Raught B, Peiretti F, Gingras AC, Livingstone M, Shahbazian D, Mayeur GL, et al. 2004. Phosphorylation of eucaryotic translation initiation factor 4B Ser422 is modulated by S6 kinases. EMBO J 23:1761-9. doi: 10.1038/sj.emboj.7600193.
31. Ruggero D, Sonenberg N. 2005. The Akt of translational control. Oncogene 24:7426-34. doi: 10.1038/sj.onc.1209098.
32. Salih DA, Brunet A. 2008. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr Opin Cell Biol 20:126-36. doi: 10.1016/j.ceb.2008.02.005.
33. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307:1098-101. doi: 10.1126/science.1106148.
34. Sengupta S, Peterson TR, Sabatini DM. 2010. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell 40:310-22. doi: 10.1016/j.molcel.2010.09.026.
35. Slack C, Giannakou ME, Foley A, Goss M, Partridge L. 2011. dFOXO-independent effects of reduced insulin-like signaling in Drosophila. Aging Cell 10:735-48. doi: 10.1111/j.1474-9726.2011.00707.x.
36. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136:731-45. doi: 10.1016/j.cell.2009.01.042.
37. Spriggs KA, Bushell M, Willis AE. 2010. Translational regulation of gene expression during conditions of cell stress. Mol Cell 40:228-37. doi: 10.1016/j.molcel.2010.09.028.
38. Spriggs KA, Cobbold LC, Jopling CL, Cooper RE, Wilson LA, Stoneley M, et al. 2009a. Canonical initiation factor requirements of the Myc family of internal ribosome entry segments. Mol Cell Biol 29:1565-74. doi: 10.1128/MCB.01283-08.
39. Spriggs KA, Cobbold LC, Ridley SH, Coldwell M, Bottley A, Bushell M, et al. 2009b. The human insulin receptor mRNA contains a functional internal ribosome entry segment. Nucleic Acids Res 37:5881-93. doi: 10.1093/nar/gkp623.
40. Svitkin YV, Herdy B, Costa-Mattioli M, Gingras AC, Raught B, Sonenberg N. 2005. Eukaryotic translation initiation factor 4E availability controls the switch between cap-dependent and internal ribosomal entry site-mediated translation. Mol Cell Biol 25:10556-65. doi: 10.1128/MCB.25.23.10556-10565.2005.
41. Teleman AA, Hietakangas V, Sayadian AC, Cohen SM. 2008. Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cell Metab 7:21-32. doi: 10.1016/j.cmet.2007.11.010.
42. Thoma C, Bergamini G, Galy B, Hundsdoerfer P, Hentze MW. 2004. Enhancement of IRES-mediated translation of the c-myc and BiP mRNAs by the poly(A) tail is independent of intact eIF4G and PABP. Mol Cell 15:925-35. doi: 10.1016/j.molcel.2004.08.021.
43. Tsukiyama-Kohara K, Iizuka N, Kohara M, Nomoto A. 1992. Internal ribosome entry site within hepatitis C virus RNA. J Virol 66:1476-83. doi: 10.1006/viro.1997.8600.
44. Wang MC, Bohmann D, Jasper H. 2005. JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121:115-25. doi: 10.1016/j.cell.2005.02.030.
45. Waters LC, Strong SL, Ferlemann E, Oka O, Muskett FW, Veverka V, et al. 2011. Structure of the tandem MA-3 region of Pdcd4 protein and characterization of its interactions with eIF4A and eIF4G: molecular mechanisms of a tumor suppressor. J Biol Chem 286:17270-80. doi: 10.1074/jbc.M110.166157.
46. Yang HS, Jansen AP, Komar AA, Zheng X, Merrick WC, Costes S, et al. 2003. The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol Cell Biol 23:26-37. doi: 10.1128/MCB.23.1.26-37.2003.
47. Zoncu R, Efeyan A, Sabatini DM. 2011. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 12:21-35. doi: 10.1038/nrm3025.