Abstract
Biotherapeutics have revolutionized modern medicine by providing medicines that would not have been possible with small molecules. With respect to cancer therapies, this represents the current sector of the pharmaceutical industry having the largest therapeutic impact, as exemplified by the development of recombinant antibodies and cell-based therapies. In cancer, one of the most common regulatory alterations is the perturbation of translational control. Among these, changes in eukaryotic initiation factor 4F (eIF4F) are associated with tumor initiation, progression, and drug resistance in a number of settings. This, coupled with the fact that systemic suppression of eIF4F appears well tolerated, indicates that therapeutic agents targeting eIF4F hold much therapeutic potential. Here, we discuss opportunities offered by biologicals for this purpose.
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Abbreviations
- eIF:
-
Eukaryotic initiation factor
- TC:
-
Ternary complex
- UTR:
-
Untranslated region
- IRES:
-
Internal ribosome entry site
- HRV:
-
Human rhinovirus
- GBM:
-
Gliobastoma multiforme
References
Hurst S (2011) Biotherapeutics Drug Development
Ltd E (2014) EvaluatePharma world preview 2014. In: Hills P (ed) Outlook to 2020
Pelletier J, Graff J, Ruggero D, Sonenberg N (2015) Targeting the eIF4F translation initiation complex: a critical nexus for cancer development. Cancer Res 75:250–263
Bhat M, Robichaud N, Hulea L, Sonenberg N, Pelletier J, Topisirovic I (2015) Targeting the translation machinery in cancer. Nat Rev Drug Discov. 14:261–278
Chu J, Cargnello M, Topisirovic I Pelletier J (2016) Translation initiation factors: reprogramming protein synthesis in cancer. Trends Cell Biol
Wek RC, Jiang HY, Anthony TG (2006) Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34:7–11
Sinvani H, Haimov O, Svitkin Y, Sonenberg N, Tamarkin-Ben-Harush A, Viollet B, Dikstein R (2015) Translational tolerance of mitochondrial genes to metabolic energy stress involves TISU and eIF1-eIF4GI cooperation in start codon selection. Cell Metab 21:479–492
Fernandez IS, Bai XC, Murshudov G, Scheres SH, Ramakrishnan V (2014) Initiation of translation by cricket paralysis virus IRES requires its translocation in the ribosome. Cell 157:823–831
Hinnebusch AG, Ivanov IP, Sonenberg N (2016) Translational control by 5′-untranslated regions of eukaryotic mRNAs. Science 352:1413–1416
Jackson RJ, Hellen CU, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11:113–127
Matthews MB, Sonenberg N, Hershey JWB (2007) Origins and principle of translation control. In: Matthews MB, Sonenberg N, Hershey JWB (eds) Translational control in biology and medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 1–40
Johnson LF, Levis R, Abelson HT, Green H, Penman S (1976) Changes in RNA in relation to growth of the fibroblast. IV. Alterations in theproduction and processing of mRNA and rRNA in resting and growing cells. J Cell Biol 71:933–938
Colina R, Costa-Mattioli M, Dowling RJ, Jaramillo M, Tai LH, Breitbach CJ, Martineau Y, Larsson O, Rong L, Svitkin YV, Makrigiannis AP, Bell JC, Sonenberg N (2008) Translational control of the innate immune response through IRF-7. Nature 452:323–328
Larsson O, Li S, Issaenko OA, Avdulov S, Peterson M, Smith K, Bitterman PB, Polunovsky VA (2007) Eukaryotic translation initiation factor 4E induced progression of primary human mammary epithelial cells along the cancer pathway is associated with targeted translational deregulation of oncogenic drivers and inhibitors. Cancer Res 67:6814–6824
Larsson O, Perlman DM, Fan D, Reilly CS, Peterson M, Dahlgren C, Liang Z, Li S, Polunovsky VA, Wahlestedt C, Bitterman PB (2006) Apoptosis resistance downstream of eIF4E: posttranscriptional activation of an anti-apoptotic transcript carrying a consensus hairpin structure. Nucleic Acids Res 34:4375–4386
Polunovsky VA, Rosenwald IB, Tan AT, White J, Chiang L, Sonenberg N, Bitterman PB (1996) Translational control of programmed cell death: eukaryotic translation initiation factor 4E blocks apoptosis in growth-factor-restricted fibroblasts with physiologically expressed or deregulated Myc. Mol Cell Biol 16:6573–6581
Kevil CG, De Benedetti A, Payne DK, Coe LL, Laroux FS, Alexander JS (1996) Translational regulation of vascular permeability factor by eukaryotic initiation factor 4E: implications for tumor angiogenesis. Int J Cancer 65:785–790
Walsh D, Mathews MB, Mohr I (2013) Tinkering with translation: protein synthesis in virus-infected cells. Cold Spring Harb Perspect Biol 5:a012351
Topisirovic I, Sonenberg N (2011) mRNA translation and energy metabolism in cancer: the role of the MAPK and mTORC1 pathways. Cold Spring Harbor symposia on quantitative biology
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674
Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70
Hinnebusch AG, Lorsch JR. The mechanism of eukaryotic translation initiation: new insights and challenges. Cold Spring Harbor Perspect Biol 4
Pestova TV, Kolupaeva VG (2002) The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev 16:2906–2922
Sonenberg N (1981) ATP/Mg++-dependent cross-linking of cap binding proteins to the 5′ end of eukaryotic mRNA. Nucleic Acids Res 9:1643–1656
Nielsen PJ, Trachsel H (1988) The mouse protein synthesis initiation factor 4A gene family includes two related functional genes which are differentially expressed. EMBO J 7:2097–2105
Galicia-Vazquez G, Cencic R, Robert F, Agenor AQ, Pelletier J (2012) A cellular response linking eIF4AI activity to eIF4AII transcription. RNA 18:1373–1384
Yoder-Hill J, Pause A, Sonenberg N, Merrick WC (1993) The p46 subunit of eukaryotic initiation factor (eIF)-4F exchanges with eIF-4A. J Biol Chem 268:5566–5573
Galicia-Vazquez G, Chu J, Pelletier J (2015) eIF4AII is dispensable for miRNA-mediated gene silencing. RNA 21:1826–1833
Williams-Hill DM, Duncan RF, Nielsen PJ Tahara SM (1997) Differential expression of the murine eukaryotic translation initiation factor isogenes eIF4A(I) and eIF4A(II) is dependent upon cellular growth status. Arch Biochem Biophys 338:111–120
Lin CJ, Cencic R, Mills JR, Robert F, Pelletier J (2008) c-Myc and eIF4F are components of a feedforward loop that links transcription and translation. Cancer Res 68:5326–5334
Imataka H, Gradi A, Sonenberg N (1998) 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 17:7480–7489
Gradi A, Imataka H, Svitkin YV, Rom E, Raught B, Morino S, Sonenberg N (1998) A novel functional human eukaryotic translation initiation factor 4G. Mol Cell Biol 18:334–342
Pyronnet S, Imataka H, Gingras AC, Fukunaga R, Hunter T, Sonenberg N (1999) Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. EMBO J 18:270–279
Ho JJ, Wang M, Audas TE, Kwon D, Carlsson SK, Timpano S, Evagelou SL, Brothers S, Gonzalgo ML, Krieger JR, Chen S, Uniacke J Lee S (2016) Systemic reprogramming of translation efficiencies on oxygen stimulus. Cell Rep 14:1293–1300
Duncan R, Milburn SC, Hershey JW (1987) Regulated phosphorylation and low abundance of HeLa cell initiation factor eIF-4F suggest a role in translational control. Heat shock effects on eIF-4F. J Biol Chem 262:380–388
Pelletier J, Sonenberg N (1985) Insertion mutagenesis to increase secondary structure within the 5′ noncoding region of a eukaryotic mRNA reduces translational efficiency. Cell 40:515–526
Pelletier J, Sonenberg N (1985) Photochemical cross-linking of cap binding proteins to eucaryotic mRNAs: effect of mRNA 5′ secondary structure. Mol Cell Biol 5:3222–3230
Lawson TG, Ray BK, Dodds JT, Grifo JA, Abramson RD, Merrick WC, Betsch DF, Weith HL, Thach RE (1986) Influence of 5′ proximal secondary structure on the translational efficiency of eukaryotic mRNAs and on their interaction with initiation factors. J Biol Chem 261:13979–13989
Babendure JR, Babendure JL, Ding JH Tsien RY (2006) Control of mammalian translation by mRNA structure near caps. RNA 12:851–861
Svitkin YV, Pause A, Haghighat A, Pyronnet S, Witherell G, Belsham GJ Sonenberg N (2001) The requirement for eukaryotic initiation factor 4A (elF4A) in translation is in direct proportion to the degree of mRNA 5′ secondary structure. RNA 7:382–394
Shah P, Ding Y, Niemczyk M, Kudla G, Plotkin JB (2013) Rate-limiting steps in yeast protein translation. Cell 153:1589–1601
Goossen B, Caughman SW, Harford JB, Klausner RD, Hentze MW (1990) Translational repression by a complex between the iron-responsive element of ferritin mRNA and its specific cytoplasmic binding protein is position-dependent in vivo. EMBO J 9:4127–4133
Lazaris-Karatzas A, Montine KS, Sonenberg N (1990) Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5′ cap. Nature 345:544–547
Ruggero D, Montanaro L, Ma L, Xu W, Londei P, Cordon-Cardo C Pandolfi PP (2004) The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat Med. 10:484–486
Wendel HG, De Stanchina E, Fridman JS, Malina A, Ray S, Kogan S, Cordon-Cardo C, Pelletier J, Lowe SW (2004) Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 428:332–337
Sonenberg N, Hinnebusch AG (2007) New modes of translational control in development, behavior, and disease. Mol Cell 28:721–729
Boussemart L et al (2014) eIF4F is a nexus of resistance to anti-BRAF and anti-MEK cancer therapies. Nature 513:105–109
Wendel HG, Malina A, Zhao Z, Zender L, Kogan SC, Cordon-Cardo C, Pelletier J, Lowe SW (2006) Determinants of sensitivity and resistance to rapamycin-chemotherapy drug combinations in vivo. Cancer Res 66:7639–7646
Ilic N, Utermark T, Widlund HR, Roberts TM (2011) PI3K-targeted therapy can be evaded by gene amplification along the MYC-eukaryotic translation initiation factor 4E (eIF4E) axis. Proc Natl Acad Sci USA 108:E699–E708
Cope CL, Gilley R, Balmanno K, Sale MJ, Howarth KD, Hampson M, Smith PD, Guichard SM, Cook SJ (2014) Adaptation to mTOR kinase inhibitors by amplification of eIF4E to maintain cap-dependent translation. J Cell Sci 127:788–800
Croft A, Tay KH, Boyd SC, Guo ST, Jiang CC, Lai F, Tseng HY, Jin L, Rizos H, Hersey P, Zhang XD (2014) Oncogenic activation of MEK/ERK primes melanoma cells for adaptation to endoplasmic reticulum stress. J Invest Dermatol 134:488–497
Gingras ACRB, Gygi SP, Niedzwiecka A, Miron M, Burley SK, Polakiewicz RD, Wyslouch-Cieszynska A, Aebersold R, Sonenberg N (2001) Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev 15:2852–2864
Yang HS, Jansen AP, Komar AA, Zheng X, Merrick WC, Costes S, Lockett SJ, Sonenberg N, Colburn NH (2003) The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol Cell Biol 23:26–37
Yang HS, Cho MH, Zakowicz H, Hegamyer G, Sonenberg N, Colburn NH (2004) A novel function of the MA-3 domains in transformation and translation suppressor Pdcd4 is essential for its binding to eukaryotic translation initiation factor 4A. Mol Cell Biol 24:3894–3906
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 314:467–471
Ma XM, Blenis J (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10:307–318
Flynn A, Proud CG (1995) Serine 209, not serine 53, is the major site of phosphorylation in initiation factor eIF-4E in serum-treated Chinese hamster ovary cells. J Biol Chem 270:21684–21688
Joshi B, Cai AL, Keiper BD, Minich WB, Mendez R, Beach CM, Stepinski J, Stolarski R, Darzynkiewicz E, Rhoads RE (1995) Phosphorylation of eukaryotic protein synthesis initiation factor 4E at Ser-209. J Biol Chem 270:14597–14603
Waskiewicz AJ, Johnson JC, Penn B, Mahalingam M, Kimball SR, Cooper JA (1999) Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol Cell Biol 19:1871–1880
Ueda T, Watanabe-Fukunaga R, Fukuyama H, Nagata S, Fukunaga R (2004) Mnk2 and Mnk1 are essential for constitutive and inducible phosphorylation of eukaryotic initiation factor 4E but not for cell growth or development. Mol Cell Biol 24:6539–6549
Furic L, Rong L, Larsson O, Koumakpayi IH, Yoshida K, Brueschke A, Petroulakis E, Robichaud N, Pollak M, Gaboury LA, Pandolfi PP, Saad F, Sonenberg N (2010) eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression. Proc Natl Acad Sci USA 107:14134–14139
Topisirovic I, Ruiz-Gutierrez M, Borden KL (2004) Phosphorylation of the eukaryotic translation initiation factor eIF4E contributes to its transformation and mRNA transport activities. Cancer Res 64:8639–8642
Wendel HG, Silva RL, Malina A, Mills JR, Zhu H, Ueda T, Watanabe-Fukunaga R, Fukunaga R, Teruya-Feldstein J, Pelletier J, Lowe SW (2007) Dissecting eIF4E action in tumorigenesis. Genes Dev 21:3232–3237
Gingras AC, Raught B, Sonenberg N (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68:913–963
Scheper GC, Proud CG (2002) Does phosphorylation of the cap-binding protein eIF4E play a role in translation initiation? Eur J Biochem 269:5350–5359
Lin CJ, Nasr Z, Premsrirut PK, Porco JA, Jr., Hippo Y, Lowe SW Pelletier J (2012) Targeting synthetic lethal interactions between Myc and the eIF4F complex impedes tumorigenesis. Cell Reports 1:325–333
Robert F, Roman W, Bramoulle A, Fellmann C, Roulston A, Shustik C, Porco JA Jr, Shore GC, Sebag M, Pelletier J (2014) Translation initiation factor eIF4F modifies the dexamethasone response in multiple myeloma. Proc Natl Acad Sci USA 111:13421–13426
Wiegering A, Uthe FW, Jamieson T, Ruoss Y, Huttenrauch M, Kuspert M, Pfann C, Nixon C, Herold S, Walz S, Taranets L, Germer CT, Rosenwald A, Sansom OJ, Eilers M (2015) Targeting translation initiation bypasses signaling crosstalk mechanisms that maintain high MYC levels in colorectal cancer. Cancer Discov 5:768–781
Beroukhim R et al (2010) The landscape of somatic copy-number alteration across human cancers. Nature 463:899–905
Gleave ME, Monia BP (2005) Antisense therapy for cancer. Nat Rev Cancer 5:468–479
Rinker-Schaeffer CW, Graff JR, De Benedetti A, Zimmer SG, Rhoads RE (1993) Decreasing the level of translation initiation factor 4E with antisense RNA causes reversal of ras-mediated transformation and tumorigenesis of cloned rat embryo fibroblasts. Int J Cancer 55:841–847
Graff JR, Boghaert ER, De Benedetti A, Tudor DL, Zimmer CC, Chan SK, Zimmer SG (1995) Reduction of translation initiation factor 4E decreases the malignancy of ras-transformed cloned rat embryo fibroblasts. Int J Cancer 60:255–263
Thumma SC, Jacobson BA, Patel MR, Konicek BW, Franklin MJ, Jay-Dixon J, Sadiq A, De A, Graff JR, Kratzke RA (2015) Antisense oligonucleotide targeting eukaryotic translation initiation factor 4E reduces growth and enhances chemosensitivity of non-small-cell lung cancer cells. Cancer Gene Ther
Altmann M, Handschin C, Trachsel H (1987) mRNA cap-binding protein: cloning of the gene encoding protein synthesis initiation factor eIF-4E from Saccharomyces cerevisiae. Mol Cell Biol 7:998–1003
Truitt ML, Conn CS, Shi Z, Pang X, Tokuyasu T, Coady AM, Seo Y, Barna M, Ruggero D (2015) Differential requirements for eIF4E dose in normal development and cancer. Cell 162:59–71
Graff JR et al (2007) Therapeutic suppression of translation initiation factor eIF4E expression reduces tumor growth without toxicity. J Clin Invest. 117:2638–2648
Hong DS, Kurzrock R, Oh Y, Wheler J, Naing A, Brail L, Callies S, Andre V, Kadam SK, Nasir A, Holzer TR, Meric-Bernstam F, Fishman M, Simon G (2011) A phase 1 dose escalation, pharmacokinetic, and pharmacodynamic evaluation of eIF-4E antisense oligonucleotide LY2275796 in patients with advanced cancer. Clin Cancer Res 17:6582–6591
Duffy AG et al (2016) Modulation of tumor eIF4E by antisense inhibition: a phase I/II translational clinical trial of ISIS 183750-an antisense oligonucleotide against eIF4E-in combination with irinotecan in solid tumors and irinotecan-refractory colorectal cancer. Int J Cancer 139:1648–1657
Mochizuki K, Oguro A, Ohtsu T, Sonenberg N, Nakamura Y (2005) High affinity RNA for mammalian initiation factor 4E interferes with mRNA-cap binding and inhibits translation. RNA 11:77–89
Oguro A, Ohtsu T, Svitkin YV, Sonenberg N, Nakamura Y (2003) RNA aptamers to initiation factor 4A helicase hinder cap-dependent translation by blocking ATP hydrolysis. RNA 9:394–407
Miyakawa S, Oguro A, Ohtsu T, Imataka H, Sonenberg N, Nakamura Y (2006) RNA aptamers to mammalian initiation factor 4G inhibit cap-dependent translation by blocking the formation of initiation factor complexes. RNA 12:1825–1834
Guo WM, Kong KW, Brown CJ, Quah ST, Yeo HL, Hoon S, Seow Y (2014) Identification and characterization of an eIF4e DNA aptamer that inhibits proliferation with high throughput sequencing. Mol Ther Nucleic Acids 3:e217
Tiedge H, Fremeau RT Jr, Weinstock PH, Arancio O, Brosius J (1991) Dendritic location of neural BC1 RNA. Proc Natl Acad Sci USA 88:2093–2097
Eom HJ, Chatterjee N, Lee J, Choi J (2014) Integrated mRNA and micro RNA profiling reveals epigenetic mechanism of differential sensitivity of Jurkat T cells to AgNPs and Ag ions. Toxicol Lett 229:311–318
Iacoangeli A, Tiedge H (2013) Translational control at the synapse: role of RNA regulators. Trends Biochem Sci 38:47–55
Eom T, Muslimov IA, Tsokas P, Berardi V, Zhong J, Sacktor TC, Tiedge H (2014) Neuronal BC RNAs cooperate with eIF4B to mediate activity-dependent translational control. J Cell Biol 207:237–252
Wang H, Iacoangeli A, Popp S, Muslimov IA, Imataka H, Sonenberg N, Lomakin IB, Tiedge H (2002) Dendritic BC1 RNA: functional role in regulation of translation initiation. J Neurosci 22:10232–10241
Lin D, Pestova TV, Hellen CUT, Tiedge H (2008) Translational control by a small RNA: dendritic BC1 RNA targets the eukaryotic initiation factor 4A helicase mechanism. Mol Cell Biol 28:3008–3019
Muddashetty R, Khanam T, Kondrashov A, Bundman M, Iacoangeli A, Kremerskothen J, Duning K, Barnekow A, Huttenhofer A, Tiedge H, Brosius J (2002) Poly(A)-binding protein is associated with neuronal BC1 and BC200 ribonucleoprotein particles. J Mol Biol 321:433–445
Lin CJ, Nasr Z, Premsrirut PK, Porco JA, Jr., Hippo Y, Lowe SW, Pelletier J (2012) Targeting synthetic lethal interactions between Myc and the eIF4F complex impedes tumorigenesis. Cell Reports 1:325–333
Soni A, Akcakanat A, Singh G, Luyimbazi D, Zheng Y, Kim D, Gonzalez-Angulo A, Meric-Bernstam F (2008) eIF4E knockdown decreases breast cancer cell growth without activating Akt signaling. Mol Cancer Ther 7:1782–1788
Oridate N, Kim HJ, Xu X, Lotan R (2005) Growth inhibition of head and neck squamous carcinoma cells by small interfering RNAs targeting eIF4E or cyclin D1 alone or combined with cisplatin. Cancer Biol Ther 4:318–323
Choi CH, Lee JS, Kim SR, Lee YY, Kim CJ, Lee JW, Kim TJ, Lee JH, Kim BG, Bae DS (2011) Direct inhibition of eIF4E reduced cell growth in endometrial adenocarcinoma. J Cancer Res Clin Oncol 137:463–469
Nasr Z, Robert F, Porco JA, Jr., Muller WJ, Pelletier J (2013) eIF4F suppression in breast cancer affects maintenance and progression. Oncogene 32:861–871
Hayman TJ, Williams ES, Jamal M, Shankavaram UT, Camphausen K, Tofilon PJ (2012) Translation initiation factor eIF4E is a target for tumor cell radiosensitization. Cancer Res 72:2362–2372
Zhou FF, Yan M, Guo GF, Wang F, Qiu HJ, Zheng FM, Zhang Y, Liu Q, Zhu XF, Xia LP (2011) Knockdown of eIF4E suppresses cell growth and migration, enhances chemosensitivity and correlates with increase in Bax/Bcl-2 ratio in triple-negative breast cancer cells. Med Oncol 28:1302–1307
Cencic R, Robert F, Galicia-Vazquez G, Malina A, Ravindar K, Somaiah R, Pierre P, Tanaka J, Deslongchamps P, Pelletier J (2013) Modifying chemotherapy response by targeted inhibition of eukaryotic initiation factor 4A. Blood Cancer J 3:e128
Carrieri C, Cimatti L, Biagioli M, Beugnet A, Zucchelli S, Fedele S, Pesce E, Ferrer I, Collavin L, Santoro C, Forrest AR, Carninci P, Biffo S, Stupka E, Gustincich S (2012) Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491:454–457
Yao Y et al (2015) RNAe: an effective method for targeted protein translation enhancement by artificial non-coding RNA with SINEB2 repeat. Nucleic Acids Res 43:e58
Hill JM, Roberts J, Loeb E, Khan A, MacLellan A, Hill RW (1967) l-Asparaginase therapy for leukemia and other malignant neoplasms. Remission in human leukemia. JAMA 202:882–888
Parmentier JH, Maggi M, Tarasco E, Scotti C, Avramis VI, Mittelman SD (2015) Glutaminase activity determines cytotoxicity of l-asparaginases on most leukemia cell lines. Leuk Res 39:757–762
Bunpo P, Dudley A, Cundiff JK, Cavener DR, Wek RC, Anthony TG (2009) GCN2 protein kinase is required to activate amino acid deprivation responses in mice treated with the anti-cancer agent l-asparaginase. J Biol Chem 284:32742–32749
Mader S, Lee H, Pause A, Sonenberg N (1995) The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Mol Cell Biol 15:4990–4997
Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK (1999) Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol Cell 3:707–716
Fletcher CM, Wagner G (1998) The interaction of eIF4E with 4E-BP1 is an induced fit to a completely disordered protein. Protein Sci 7:1639–1642
Yang H, Li LW, Shi M, Wang JH, Xiao F, Zhou B, Diao LQ, Long XL, Liu XL, Xu L (2012) In vivo study of breast carcinoma radiosensitization by targeting eIF4E. Biochem Biophys Res Commun 423:878–883
Rousseau D, Gingras AC, Pause A, Sonenberg N (1996) The eIF4E-binding proteins 1 and 2 are negative regulators of cell growth. Oncogene 13:2415–2420
Li S, Sonenberg N, Gingras AC, Peterson M, Avdulov S, Polunovsky VA, Bitterman PB (2002) Translational control of cell fate: availability of phosphorylation sites on translational repressor 4E-BP1 governs its proapoptotic potency. Mol Cell Biol 22:2853–2861
Jiang H, Coleman J, Miskimins R, Miskimins WK (2003) Expression of constitutively active 4EBP-1 enhances p27Kip1 expression and inhibits proliferation of MCF7 breast cancer cells. Cancer Cell Int 3:2
Lynch M, Fitzgerald C, Johnston KA, Wang S, Schmidt EV (2004) Activated eIF4E-binding protein slows G1 progression and blocks transformation by c-myc without inhibiting cell growth. J Biol Chem 279:3327–3339
Herbert TP, Fahraeus R, Prescott A, Lane DP, Proud CG (2000) Rapid induction of apoptosis mediated by peptides that bind initiation factor eIF4E. Curr Biol 10:793–796
Ko SY, Guo H, Barengo N, Naora H (2009) Inhibition of ovarian cancer growth by a tumor-targeting peptide that binds eukaryotic translation initiation factor 4E. Clin Cancer Res 15:4336–4347
Zhou W, Quah ST, Verma CS, Liu Y, Lane DP, Brown CJ (2012) Improved eIF4E binding peptides by phage display guided design: plasticity of interacting surfaces yield collective effects. PLoS One 7:e47235
Lama D, Quah ST, Verma CS, Lakshminarayanan R, Beuerman RW, Lane DP, Brown CJ (2013) Rational optimization of conformational effects induced by hydrocarbon staples in peptides and their binding interfaces. Sci Rep 3:3451
Brown CJ, Lim JJ, Leonard T, Lim HC, Chia CS, Verma CS, Lane DP (2011) Stabilizing the eIF4G1 alpha-helix increases its binding affinity with eIF4E: implications for peptidomimetic design strategies. J Mol Biol 405:736–753
Brown CJ, Dastidar SG, See HY, Coomber DW, Ortiz-Lombardia M, Verma C, Lane DP (2010) Rational design and biophysical characterization of thioredoxin-based aptamers: insights into peptide grafting. J Mol Biol 395:871–883
Yang HS, Knies JL, Stark C, Colburn NH (2003) Pdcd4 suppresses tumor phenotype in JB6 cells by inhibiting AP-1 transactivation. Oncogene 22:3712–3720
Eberle J, Fecker LF, Bittner JU, Orfanos CE, Geilen CC (2002) Decreased proliferation of human melanoma cell lines caused by antisense RNA against translation factor eIF-4A1. Br J Cancer 86:1957–1962
Jansen AP, Camalier CE, Colburn NH (2005) Epidermal expression of the translation inhibitor programmed cell death 4 suppresses tumorigenesis. Cancer Res 65:6034–6041
Kim YK, Minai-Tehrani A, Lee JH, Cho CS, Cho MH, Jiang HL (2013) Therapeutic efficiency of folated poly(ethylene glycol)-chitosan-graft-polyethylenimine-Pdcd4 complexes in H-ras12V mice with liver cancer. Int J Nanomed 8:1489–1498
Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S, Allgayer H (2008) MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27:2128–2136
Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY (2008) MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18:350–359
Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH (2008) Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem 283:1026–1033
Pause A, Methot N, Svitkin Y, Merrick WC, Sonenberg N (1994) Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4F in cap-dependent and cap-independent initiation of translation. EMBO J 13:1205–1215
Cruz-Migoni A et al (2011) A Burkholderia pseudomallei toxin inhibits helicase activity of translation factor eIF4A. Science 334:821–824
Konicek BW et al (2011) Therapeutic inhibition of MAP kinase interacting kinase blocks eukaryotic initiation factor 4E phosphorylation and suppresses outgrowth of experimental lung metastases. Cancer Res 71:1849–1857
Robichaud N, Del Rincon SV, Huor B, Alain T, Petruccelli LA, Hearnden J, Goncalves C, Grotegut S, Spruck CH, Furic L, Larsson O, Muller WJ, Miller WH, Sonenberg N (2014) Phosphorylation of eIF4E promotes EMT and metastasis via translational control of SNAIL and MMP-3. Oncogene
Cuesta R, Xi Q, Schneider RJ (2000) Adenovirus-specific translation by displacement of kinase Mnk1 from cap-initiation complex eIF4F. EMBO J 19:3465–3474
Cuesta R, Xi Q, Schneider RJ (2004) Structural basis for competitive inhibition of eIF4G-Mnk1 interaction by the adenovirus 100-kilodalton protein. J Virol 78:7707–7716
Gromeier M, Lachmann S, Rosenfeld MR, Gutin PH, Wimmer E (2000) Intergeneric poliovirus recombinants for the treatment of malignant glioma. Proc Natl Acad Sci USA 97:6803–6808
Gromeier M, Alexander L, Wimmer E (1996) Internal ribosomal entry site substitution eliminates neurovirulence in intergeneric poliovirus recombinants. Proc Natl Acad Sci USA 93:2370–2375
Gromeier M, Bossert B, Arita M, Nomoto A, Wimmer E (1999) Dual stem loops within the poliovirus internal ribosomal entry site control neurovirulence. J Virol 73:958–964
Merrill MK, Gromeier M (2006) The double-stranded RNA binding protein 76:NF45 heterodimer inhibits translation initiation at the rhinovirus type 2 internal ribosome entry site. J Virol 80:6936–6942
Merrill MK, Dobrikova EY, Gromeier M (2006) Cell-type-specific repression of internal ribosome entry site activity by double-stranded RNA-binding protein 76. J Virol 80:3147–3156
Gradi A, Svitkin YV, Imataka H, Sonenberg N (1998) Proteolysis of human eukaryotic translation initiation factor eIF4GII, but not eIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection. Proc Natl Acad Sci USA 95:11089–11094
Dobrikova EY, Goetz C, Walters RW, Lawson SK, Peggins JO, Muszynski K, Ruppel S, Poole K, Giardina SL, Vela EM, Estep JE, Gromeier M (2012) Attenuation of neurovirulence, biodistribution, and shedding of a poliovirus:rhinovirus chimera after intrathalamic inoculation in Macaca fascicularis. J Virol 86:2750–2759
Dobrikova EY, Broadt T, Poiley-Nelson J, Yang X, Soman G, Giardina S, Harris R, Gromeier M (2008) Recombinant oncolytic poliovirus eliminates glioma in vivo without genetic adaptation to a pathogenic phenotype. Mol Ther J Am Soc Gene Ther 16:1865–1872
Goetz C, Everson RG, Zhang LC, Gromeier M (2010) MAPK signal-integrating kinase controls cap-independent translation and cell type-specific cytotoxicity of an oncolytic poliovirus. Mol Ther J Am Soc Gene Ther 18:1937–1946
Mateyak MK, Kinzy TG (2013) ADP-ribosylation of translation elongation factor 2 by diphtheria toxin in yeast inhibits translation and cell separation. J Biol Chem 288:24647–24655
Acknowledgements
JS is supported by a Charlotte and Leo Karassik Postdoctoral Fellowship. Work in the author’s lab on eIF4F is supported by a grant from the Canadian Institutes of Health Research [CIHR # G243873].
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Steinberger, J., Chu, J., Maïga, R.I. et al. Developing anti-neoplastic biotherapeutics against eIF4F. Cell. Mol. Life Sci. 74, 1681–1692 (2017). https://doi.org/10.1007/s00018-016-2430-8
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DOI: https://doi.org/10.1007/s00018-016-2430-8