2,775
Views
18
CrossRef citations to date
0
Altmetric
Research Papers

Small molecule inhibitors of IRES-mediated translation

, , , , &
Pages 1471-1485 | Received 11 Mar 2015, Accepted 03 Jul 2015, Published online: 14 Sep 2015

References

  • Baird SD, Turcotte M, Korneluk RG, Holcik M. Searching for IRES. RNA 2006; 12: 1755-85; PMID:16957278; http://dx.doi.org/10.1261/rna.157806
  • Prats AC, Prats H. Translational control of gene expression: role of IRESs and consequences for cell transformation and angiogenesis. Prog. Nucleic Acid Res Mol Biol 2002; 72: 367-413; http://dx.doi.org/10.1016/S0079-6603(02)72075-8
  • Marash L, Liberman N, Henis-Korenblit S, Sivan G, Reem E, Elroy-Stein O, Kimchi A. DAP5 promotes cap-independent translation of Bcl-2 and CDK1 to facilitate cell survival during mitosis. Mol Cell 2008; 30: 447-59; PMID:18450493; http://dx.doi.org/10.1016/j.molcel.2008.03.018
  • Majumder M, Yaman I, Gaccioli F, Zeenko VV, Wang C, Caprara MG, Venema RC, Komar AA, Snider MD, Hatzoglou M. The hnRNA-binding proteins hnRNP L and PTB are required for efficient translation of the Cat-1 arginine/lysine transporter mRNA during amino acid starvation. Mol Cell Biol 2009; 29:2899-912; PMID:19273590; http://dx.doi.org/10.1128/MCB.01774-08
  • 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; 13:1792-1801; PMID:12006670; http://dx.doi.org/10.1091/mbc.02-02-0017
  • Riley A, Jordan LE, Holcik M. Distinct 5′ UTRs regulate XIAP expression under normal growth conditions and during cellular stress. Nucleic Acids Res 2010; 38:4665-74; PMID:20385593; http://dx.doi.org/10.1093/nar/gkq241
  • Komar AA, Hatzoglou M. Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 2011; 10:229-40; PMID:21220943; http://dx.doi.org/10.4161/cc.10.2.14472
  • Komar AA, Mazumder B, Merrick WC. A new framework for understanding IRES-mediated translation. Gene 2012; 502:75-86; PMID:22555019; http://dx.doi.org/10.1016/j.gene.2012.04.039
  • Fernandez J, Yaman I, Mishra R, Merrick WC, Snider MD, Lamers WH, Hatzoglou M. Internal ribosome entry site-mediated translation of a mammalian mRNA is regulated by amino acid availability. J Biol Chem 2001; 276:12285-91; PMID:11114306; http://dx.doi.org/10.1074/jbc.M009714200
  • Morrish BC, Rumsby MG. The 5′ untranslated region of protein kinase Cdelta directs translation by an internal ribosome entry segment that is most active in densely growing cells and during apoptosis. Mol Cell Biol 2002; 22:6089-99; PMID:12167703; http://dx.doi.org/10.1128/MCB.22.17.6089-6099.2002
  • 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; PMID:15123638; http://dx.doi.org/10.1074/jbc.M402727200
  • Eto I. Upstream molecular signaling pathways of p27(Kip1) expression: effects of 4-hydroxytamoxifen, dexamethasone, and retinoic acids. Cancer Cell Int 2010; 10:3; PMID:20170512; http://dx.doi.org/10.1186/1475-2867-10-3
  • Jimenez J, Jang GM, Semler BL, Waterman ML. An internal ribosome entry site mediates translation of lymphoid enhancer factor-1. RNA 2005; 11:1385-99; PMID:16120831; http://dx.doi.org/10.1261/rna.7226105
  • Petz M, Them N, Huber H, Beug H, Mikulits W. La enhances IRES-mediated translation of laminin B1 during malignant epithelial to mesenchymal transition. Nucleic Acids Res 2012; 40: 290-302; PMID:21896617; http://dx.doi.org/10.1093/nar/gkr717
  • Pozner A, Goldenberg D, Negreanu V, Le SY, Elroy-Stein O, Levanon D, Groner Y. Transcription-coupled translation control of AML1/RUNX1 is mediated by cap- and internal ribosome entry site-dependent mechanisms. Mol Cell Biol 2000; 20:2297-307; PMID:10713153; http://dx.doi.org/10.1128/MCB.20.7.2297-2307.2000
  • Yoon A, Peng G, Brandenburger Y, Zollo O, Xu W, Rego E, Ruggero D. Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science 2006; 312:902-6; PMID:16690864; http://dx.doi.org/10.1126/science.1123835
  • Zheng Y, Miskimins WK. Far upstream element binding protein 1 activates translation of p27Kip1 mRNA through its internal ribosomal entry site. Int J Biochem Cell Biol 2011; 43:1641-8; PMID:21855647; http://dx.doi.org/10.1016/j.biocel.2011.08.001
  • Nagamachi A, Htun PW, Ma F, Miyazaki K, Yamasaki N, Kanno M, Inaba T, Honda Z, Okuda T, Oda H, Tsuji K, Honda H. A 5′ untranslated region containing the IRES element in the Runx1 gene is required for angiogenesis, hematopoiesis and leukemogenesis in a knock-in mouse model. Dev Biol 2010; 345:226-36; PMID:20647008; http://dx.doi.org/10.1016/j.ydbio.2010.07.015
  • Galy B, Maret A, Prats AC, Prats H. Cell transformation results in the loss of the density-dependent translational regulation of the expression of fibroblast growth factor 2 isoforms. Cancer Res 1999; 59:165-71; PMID:9892202
  • Bonnal S, Schaeffer C, Créancier L, Clamens S, Moine H, Prats AC, Vagner S. A single internal ribosome entry site containing a G quartet RNA structure drives fibroblast growth factor 2 gene expression at four alternative translation initiation codons. J Biol Chem 2003; 278:39330-6; PMID:12857733; http://dx.doi.org/10.1074/jbc.M305580200
  • Durie D, Lewis SM, Liwak U, Kisilewicz M, Gorospe M, Holcik M. RNA-binding protein HuR mediates cytoprotection through stimulation of XIAP translation. Oncogene 2011; 30:1460-9; PMID:21102524; http://dx.doi.org/10.1038/onc.2010.527
  • Huez I, Créancier L, Audigier S, Gensac MC, Prats AC, Prats H. Two independent internal ribosome entry sites are involved in translation initiation of vascular endothelial growth factor mRNA. Mol Cell Biol 1998; 18:6178-90; PMID:9774635
  • Le Quesne JP, Stoneley M, Fraser GA, Willis AE. Derivation of a structural model for the c-myc IRES. J Mol Biol 2001; 310:111-26; PMID:11419940; http://dx.doi.org/10.1006/jmbi.2001.4745
  • Riley A, Jordan LE, Holcik M. Distinct 5′ UTRs regulate XIAP expression under normal growth conditions and during cellular stress. Nucleic Acids Res 2010; 38:4665-74; PMID:20385593; http://dx.doi.org/10.1093/nar/gkq241
  • Shi Y, Frost P, Hoang B, Benavides A, Gera J, Lichtenstein A. IL-6-induced enhancement of c-Myc translation in multiple myeloma cells: critical role of cytoplasmic localization of the rna-binding protein hnRNP A1. J Biol Chem 2011; 286:67-78; PMID:20974848; http://dx.doi.org/10.1074/jbc.M110.153221
  • Bellodi C, Krasnykh O, Haynes N, Theodoropoulou M, Peng G, Montanaro L, Ruggero D. Loss of function of the tumor suppressor DKC1 perturbs p27 translation control and contributes to pituitary tumorigenesis. Cancer Res 2010; 70:6026-35; PMID:20587522; http://dx.doi.org/10.1158/0008-5472.CAN-09-4730
  • Blau L, Knirsh R, Ben-Dror I, Oren S, Kuphal S, Hau P, Proescholdt M, Bosserhoff AK, Vardimon L. Aberrant expression of c-Jun in glioblastoma by internal ribosome entry site (IRES)-mediated translational activation. Proc Natl Acad Sci USA 2012; 109:E2875-84; PMID:23027969; http://dx.doi.org/10.1073/pnas.1203659109
  • Blume SW, Jackson NL, Frost AR, Grizzle WE, Shcherbakov OD, Choi H, Meng Z. Northwestern profiling of potential translation-regulatory proteins in human breast epithelial cells and malignant breast tissues: evidence for pathological activation of the IGF1R IRES. Exp Mol Pathol 2010; 88:341-52; PMID:20233590; http://dx.doi.org/10.1016/j.yexmp.2010.03.006
  • Dobson T, Chen J, Krushel LA. Dysregulating IRES-dependent translation contributes to over-expression of the Aurora A kinase onco-protein. Mol Cancer Res 2013; 11:887-900; PMID:23661421; http://dx.doi.org/10.1158/1541-7786.MCR-12-0707
  • Warnakulasuriyarachchi D, Cerquozzi S, Cheung HH, Holcík M. Translational induction of the inhibitor of apoptosis protein HIAP2 during endoplasmic reticulum stress attenuates cell death and is mediated via an inducible internal ribosome entry site element. J Biol Chem 2004; 279:17148-57; PMID:14960583; http://dx.doi.org/10.1074/jbc.M308737200
  • Meng Z, Jackson NL, Choi H, King PH, Emanuel PD, Blume SW. 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 2008; 217:172-83; PMID:18452152; http://dx.doi.org/10.1002/jcp.21486
  • Meng Z, King PH, Nabors LB, Jackson NL, Chen C-Y, Emanuel PD, Blume SW. The ELAV RNA-stability factor HuR binds the 5′-Untranslated region of the human IGF1R transcript and differentially represses cap-dependent and IRES-mediated translation. Nucleic Acids Res 2005; 33:2962-79; PMID:15914670; http://dx.doi.org/10.1093/nar/gki603
  • Meng Z, Jackson NL, Shcherbakov OD, Choi H, Blume SW. The human IGF1R IRES likely operates through a Shine-Dalgarno-like interaction with the G961 loop (E-site) of the 18S rRNA and is kinetically modulated by a naturally-polymorphic polyU loop. J Cell Biochem 2010; 110:531-44; PMID:20432247; http://dx.doi.org/10.1002/jcb.22569
  • Johannes G, Carter MS, Eisen MB, Brown PO, Sarnow P. Identification of eukaryotic mRNAs that are translated at reduced cap binding complex eIF4F concentrations using a cDNA microarray. Proc Natl Acad Sci U S A 1999; 96:13118-23; PMID:10557283; http://dx.doi.org/10.1073/pnas.96.23.13118
  • Spriggs KA, Stoneley M, Bushell M, Willis AE. Re-programming of translation following cell stress allows IRES-mediated translation to predominate. Biol Cell 2008; 100:27-38; PMID:18072942; http://dx.doi.org/10.1042/BC20070098
  • Beltran PJ, Mitchell P, Chung YA, Cajulis E, Lu J, Belmontes B, Ho J, Tsai MM, Zhu M, Vonderfecht S, Baserga R, Kendall R, Radinsky R, Calzone FJ. AMG 479, a fully human anti-insulin-like growth factor receptor type I monoclonal antibody, inhibits the growth and survival of pancreatic carcinoma cells. Mol Cancer Ther 2009; 8:1095-105; PMID:19366899; http://dx.doi.org/10.1158/1535-7163.MCT-08-1171
  • Zeng X, Sachdev D, Zhang H, Gaillard-Kelly M, Yee D. Sequencing of type I insulin-like growth factor receptor inhibition affects chemotherapy response in vitro and in vivo. Clin Cancer Res 2009; 15:2840-9; PMID:19351773; http://dx.doi.org/10.1158/1078-0432.CCR-08-1401
  • Stoneley M, Chappell SA, Jopling CL, Dickens M, MacFarlane M, Willis AE. c-Myc protein synthesis is initiated from the internal ribosome entry segment during apoptosis. Mol Cell Biol 2000; 20:1162-9; PMID:10648601; http://dx.doi.org/10.1128/MCB.20.4.1162-1169.2000
  • Créancier L, Mercier P, Prats AC, Morello D. c-myc Internal ribosome entry site activity is developmentally controlled and subjected to a strong translational repression in adult transgenic mice. Mol Cell Biol 2001; 21:1833-40; http://dx.doi.org/10.1128/MCB.21.5.1833-1840.2001
  • Benassayag C, Montero L, Colombié N, Gallant P, Cribbs D, Morello D. Human c-Myc isoforms differentially regulate cell growth and apoptosis in Drosophila melanogaster. Mol Cell Biol 2005; 25:9897-909; PMID:16260605; http://dx.doi.org/10.1128/MCB.25.22.9897-9909.2005
  • Hann SR, King MW, Bentley DL, Anderson CW, Eisenman RN. A non-AUG translational initiation in c-myc exon 1 generates an N-terminally distinct protein whose synthesis is disrupted in Burkitt's lymphomas. Cell 1988; 52:185-95; PMID:3277717; http://dx.doi.org/10.1016/0092-8674(88)90507-7
  • Hann SR, Sloan-Brown K, Spotts GD. Translational activation of the non-AUG-initiated c-myc 1 protein at high cell densities due to methionine deprivation. Genes Dev 1992; 6:1229-40; PMID:1628829; http://dx.doi.org/10.1101/gad.6.7.1229
  • Cowling VH. Regulation of mRNA cap methylation. Biochem J 2009; 425:295-302; PMID:20025612; http://dx.doi.org/10.1042/BJ20091352
  • Nanbru C, Lafon I, Audigier S, Gensac MC, Vagner S, Huez G, Prats AC. Alternative translation of the proto-oncogene c-myc by an internal ribosome entry site. J Biol Chem 1997; 272:32061-6; PMID:9405401; http://dx.doi.org/10.1074/jbc.272.51.32061
  • Shi Y, Sharma A, Wu H, Lichtenstein A, Gera J. Cyclin D1 and c-myc internal ribosome entry site (IRES)-dependent translation is regulated by AKT activity and enhanced by rapamycin through a p38 MAPK- and ERK-dependent pathway. J Biol Chem 2005; 280:10964-73; PMID:15634685; http://dx.doi.org/10.1074/jbc.M407874200
  • Bentley DL, Groudine M. Novel promoter upstream of the human c-myc gene and regulation of c-myc expression in B-cell lymphomas. Mol Cell Biol 1986; 6:3481-9; PMID:3540591
  • Eick D, Polack A, Kofler E, Lenoir GM, Rickinson AB, Bornkamm GW. Expression of P0- and P3-RNA from the normal and translocated c-myc allele in Burkitt's lymphoma cells. Oncogene 1990; 5:1397-402; PMID:2216463
  • Hoover RG, Kaushal V, Lary C, Travis P, Sneed T. c-myc transcription is initiated from P0 in 70% of patients with multiple myeloma. Curr Top Microbiol Immunol 1995; 194:257-64; PMID:7895497
  • Bentley DL, Groudine M. A block to elongation is largely responsible for decreased transcription of c-myc in differentiated HL60 cells. Nature 1986; 321:702-6; PMID:3520340; http://dx.doi.org/10.1038/321702a0
  • Lang JC, Wilkie NM, Clark AM, Chudleigh A, Talbot S, Whitelaw B, Frame MC. Regulatory domains within the P0 promoter of human c-myc. Oncogene 1991; 6:2067-75; PMID:1945411
  • Pullner A, Mautner J, Albert T, Eick D. Nucleosomal structure of active and inactive c-myc genes. J Biol Chem 1996; 271:31452-7; PMID:8940157; http://dx.doi.org/10.1074/jbc.271.49.31452
  • Miller TL, Huzel NJ, Davie JR, Murphy LC. C-myc gene chromatin of estrogen receptor positive and negative breast cancer cells. Mol Cell Endocrinol 1993; 91:83-9; PMID:8472857; http://dx.doi.org/10.1016/0303-7207(93)90258-L
  • De Benedetti A, Harris AL. eIF4E expression in tumors: its possible role in progression of malignancies. Int J Biochem Cell Biol 1999; 31:59-72; PMID:10216944; http://dx.doi.org/10.1016/S1357-2725(98)00132-0
  • Chappell SA, LeQuesne JP, Paulin FE, deSchoolmeester ML, Stoneley M, Soutar RL, Ralston SH, Helfrich MH, Willis AE. A mutation in the c-myc-IRES leads to enhanced internal ribosome entry in multiple myeloma: a novel mechanism of oncogene de-regulation. Oncogene 2000; 19:4437-40; PMID:10980620; http://dx.doi.org/10.1038/sj.onc.1203791
  • Cobbold LC, Spriggs KA, Haines SJ, Dobbyn HC, Hayes C, de Moor CH, Lilley KS, Bushell M, Willis AE. Identification of internal ribosome entry segment (IRES)-trans-acting factors for the Myc family of IRESs. Mol Cell Biol 2008; 28:40-9; PMID:17967896; http://dx.doi.org/10.1128/MCB.01298-07
  • Carboni JM, Wittman M, Yang Z, Lee F, Greer A, Hurlburt W, Hillerman S, Cao C, Cantor GH, Dell-John J, et al. BMS-754807, a small molecule inhibitor of insulin-like growth factor-1R/IR. Mol Cancer Ther 2009; 8:3341-9; PMID:19996272; http://dx.doi.org/10.1158/1535-7163.MCT-09-0499
  • Litzenburger BC, Creighton CJ, Tsimelzon A, Chan BT, Hilsenbeck SG, Wang T, Carboni JM, Gottardis MM, Huang F, Chang JC, et al. High IGF-IR activity in triple-negative breast cancer cell lines and tumorgrafts correlates with sensitivity to anti-IGF-IR therapy. Clin Cancer Res 2011; 17:2314-27; PMID:21177763; http://dx.doi.org/10.1158/1078-0432.CCR-10-1903
  • Turner BC, Haffty BG, Narayanan L, Yuan J, Havre PA, Gumbs AA, Kaplan L, Burgaud JL, Carter D, Baserga R. et al. Insulin-like growth factor-I receptor overexpression mediates cellular radioresistance and local breast cancer recurrence after lumpectomy and radiation. Cancer Res 1997; 57:3079-83; PMID:9242428
  • Scotlandi K, Avnet S, Benini S, Manara MC, Serra M, Cerisano V, Perdichizzi S, Lollini PL, De Giovanni C, Landuzzi L. et al.. Expression of an IGF-I receptor dominant negative mutant induces apoptosis, inhibits tumorigenesis and enhances chemosensitivity in Ewing's sarcoma cells. Int J Cancer 2002; 101:11-16; PMID:12209582; http://dx.doi.org/10.1002/ijc.10537
  • Sachdev D, Hartell JS, Lee AV, Zhang X, Yee D. A dominant negative type I insulin-like growth factor receptor inhibits metastasis of human cancer cells. J Biol Chem 2004; 279: 5017-24; PMID:14615489; http://dx.doi.org/10.1074/jbc.M305403200
  • Yanochko GM, Eckhart W. Type I insulin-like growth factor receptor over-expression induces proliferation and anti-apoptotic signaling in a three-dimensional culture model of breast epithelial cells. Breast Cancer Res 2006: 8:R18; PMID:16584539; http://dx.doi.org/10.1186/bcr1392
  • Jones RA, Campbell CI, Gunther EJ, Chodosh LA, Petrik JJ, Khokha R, Moorehead RA. Transgenic overexpression of IGF-IR disrupts mammary ductal morphogenesis and induces tumor formation. Oncogene 2007; 26:1636-44; PMID:16953219; http://dx.doi.org/10.1038/sj.onc.1209955
  • Elenbaas B, Spirio L, Koerner F, Fleming MD, Zimonjic DB, Donaher JL, Popescu NC, Hahn WC, Weinberg RA. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev 2001; 15:50-65; PMID:11156605; http://dx.doi.org/10.1101/gad.828901
  • Notari M, Neviani P, Santhanam R, Blaser BW, Chang JS, Galietta A, Willis AE, Roy DC, Caligiuri MA, Marcucci G, Perrotti D. A MAPK/HNRPK pathway controls BCR/ABL oncogenic potential by regulating MYC mRNA translation. Blood 2006; 107:2507-16; PMID:16293596; http://dx.doi.org/10.1182/blood-2005-09-3732
  • Alles MC, Gardiner-Garden M, Nott DJ, Wang Y, Foekens JA, Sutherland RL, Musgrove EA, Ormandy CJ. Meta-analysis and gene set enrichment relative to er status reveal elevated activity of MYC and E2F in the “basal” breast cancer subgroup. PLoS One 2009; 4:e4710; PMID:19270750; http://dx.doi.org/10.1371/journal.pone.0004710
  • Chandriani S, Frengen E, Cowling VH, Pendergrass SA, Perou CM, Whitfield ML, Cole MD. A core MYC gene expression signature is prominent in basal-like breast cancer but only partially overlaps the core serum response. PLoS One 2009; 4:e6693; PMID:19690609; http://dx.doi.org/10.1371/journal.pone.0006693
  • Wang J, Wang H, Li Z, Wu Q, Lathia JD, McLendon RE, Hjelmeland AB, Rich JN. c-Myc is required for maintenance of glioma cancer stem cells. PLoS One 2008; 3:e3769; PMID:19020659; http://dx.doi.org/10.1371/journal.pone.0003769
  • Cencig S, Nanbru C, Le SY, Gueydan C, Huez G, Kruys V. Mapping and characterization of the minimal internal ribosome entry segment in the human c-myc mRNA 5′ untranslated region. Oncogene 2004; 23:267-77; PMID:14712232; http://dx.doi.org/10.1038/sj.onc.1207017
  • Lynch SR, Puglisi JD. Structural origins of aminoglycoside specificity for prokaryotic ribosomes. J Mol Biol 2001; 306:1037-58; PMID:11237617; http://dx.doi.org/10.1006/jmbi.2000.4420
  • Hansen JL, Moore PB, Steitz TA. Structures of five antibiotics bound to the peptidyl transferase center of the large ribosomal subunit. J Mol Biol 2003; 330:1061-75; PMID:12860128; http://dx.doi.org/10.1016/S0022-2836(03)00668-5
  • Spriggs KA, Cobbold LC, Ridley SH, Coldwell M, Bottley A, Bushell M, Willis AE, Siddle K. The human insulin receptor mRNA contains a functional internal ribosome entry segment. Nucleic Acids Res 2009; 37:5881-93; PMID:19654240; http://dx.doi.org/10.1093/nar/gkp623
  • Olson CM, Donovan MR, Spellberg MJ, Marr MT 2nd. The insulin receptor cellular IRES confers resistance to eIF4A inhibition. Elife 2013; 2:e00542; PMID:23878722
  • Choi H, Jackson NL, Shaw DR, Emanuel PD, Liu YL, Tousson A, Meng Z, Blume SW. mrtl – a translation / localization regulatory protein encoded within the human c-myc locus and distributed throughout the endoplasmic and nucleoplasmic reticular network. J Cell Biochem 2008; 105:1092-108; also GenBank: BK006467; PMID:18816594; http://dx.doi.org/10.1002/jcb.21909
  • Gazin C, Dupont de Dinechin S, Hampe A, Masson JM, Martin P, Stehelin D, Galibert F. Nucleotide sequence of the human c-myc locus: provocative open reading frame within the first exon. EMBO J 1984; 3:383-7; PMID:6714223