Phosphorylation of eIF4E confers resistance to cellular stress and DNA-damaging agents through an interaction with 4E-T: A Rationale for novel therapeutic approaches

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Martínez, Alba ^a   Sesé, Marta ^a   Losa, Javier Hernandez ^b   Robichaud, Nathaniel ^c   Sonenberg, Nahum ^c   Aasen, Trond ^a   Ramón Y Cajal, Santiago ^a,b  

^a HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC TRIOXIDE; CARRIER PROTEIN; CGP 57380; CISPLATIN; CYCLIN D1; EUKARYOTIC TRANSLATION INITIATION FACTOR 4E NUCLEAR IMPORT FACTOR 1; GLUCOSE; GLUTAMINE; GREEN FLUORESCENT PROTEIN; HUR PROTEIN; INITIATION FACTOR 4E; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MUTANT PROTEIN; PROTEIN MCL 1; RETROVIRUS VECTOR; UNCLASSIFIED DRUG; ANILINE DERIVATIVE; ARSENOUS ACID DERIVATIVE; DNA; EIF4ENIF1 PROTEIN, HUMAN; ELAV LIKE PROTEIN 1; ELAVL1 PROTEIN, MOUSE; MCL1 PROTEIN, MOUSE; MKNK1 PROTEIN, MOUSE; MKNK2 PROTEIN, MOUSE; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; PURINE DERIVATIVE;

ANIMAL CELL; ARTICLE; BREAST CARCINOMA; CANCER CELL LINE; CELL INCLUSION; CELL STARVATION; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; FIBROBLAST; GENE SILENCING; HELA CELL LINE; HUMAN; HUMAN CELL; IMMORTALIZED CELL LINE; IN VITRO STUDY; KERATINOCYTE; KNOCKOUT MOUSE; MDA MB 231 CELL LINE; MDA MB 468 CELL LINE; MOUSE; NONHUMAN; OXIDATIVE STRESS; POLYSOME; PROCEDURES CONCERNING CELLS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; STARVATION; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CELL PROLIFERATION; CHEMISTRY; DEFICIENCY; DRUG EFFECTS; GENETICS; METABOLISM; PHOSPHORYLATION; SITE DIRECTED MUTAGENESIS;

EUKARYOTA; MUS;

ANILINE COMPOUNDS; ANIMALS; ARSENITES; CELL LINE; CELL PROLIFERATION; CISPLATIN; CYCLIN D1; DNA; DNA DAMAGE; ELAV-LIKE PROTEIN 1; EUKARYOTIC INITIATION FACTOR-4E; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; MUTAGENESIS, SITE-DIRECTED; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; PURINES;

EID: 84928748405     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123352     Document Type: Article

References (56)

1. 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. PMID: 3793730
2. Sonenberg N, Gingras AC (1998) The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Curr Opin Cell Biol 10: 268-275. PMID: 9561852
3. Rousseau D, Kaspar R, Rosenwald I, Gehrke L, Sonenberg N (1996) Translation initiation of ornithine decarboxylase and nucleocytoplasmic transport of cyclin D1 mRNA are increased in cells overexpressing eukaryotic initiation factor 4E. Proc Natl Acad Sci U S A 93: 1065-1070. PMID: 8577715
4. Culjkovic B, Topisirovic I, Skrabanek L, Ruiz-Gutierrez M, Borden KL (2006) eIF4E is a central node of an RNA regulon that governs cellular proliferation. J Cell Biol 175: 415-426. PMID: 17074885
5. Dostie J, Ferraiuolo M, Pause A, Adam SA, Sonenberg N (2000) A novel shuttling protein, 4E-T, mediates the nuclear import of the mRNA 5′ cap-binding protein, eIF4E. EMBO J 19: 3142-3156. PMID: 10856257
6. De Benedetti A, Rhoads RE (1990) Overexpression of eukaryotic protein synthesis initiation factor 4E in HeLa cells results in aberrant growth and morphology. Proc Natl Acad Sci U S A 87: 8212-8216. PMID: 2122455
7. Yoshizawa A, Fukuoka J, Shimizu S, Shilo K, Franks TJ, et al. (2010) Overexpression of phosphoeIF4E is associated with survival through AKT pathway in non-small cell lung cancer. Clin Cancer Res 16: 240-248. doi: 10.1158/1078-0432.CCR-09-0986 PMID: 20008839
8. Kerekatte V, Smiley K, Hu B, Smith A, Gelder F, et al. (1995) The proto-oncogene/translation factor eIF4E: a survey of its expression in breast carcinomas. Int J Cancer 64: 27-31. PMID: 7665244
9. 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. PMID: 2348862
10. Larsson O, Li S, Issaenko OA, Avdulov S, Peterson M, et al. (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. PMID: 17638893
11. Lazaris-Karatzas A, Smith MR, Frederickson RM, Jaramillo ML, Liu YL, et al. (1992) Ras mediates translation initiation factor 4E-induced malignant transformation. Genes Dev 6: 1631-1642. PMID: 1516827
12. Waskiewicz AJ, Flynn A, Proud CG, Cooper JA (1997) Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J 16: 1909-1920. PMID: 9155017
13. Fukunaga R, Hunter T (1997) MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J 16: 1921-1933. PMID: 9155018
14. Joshi B, Cai AL, Keiper BD, Minich WB, Mendez R, et al. (1995) Phosphorylation of eukaryotic protein synthesis initiation factor 4E at Ser-209. J Biol Chem 270: 14597-14603. PMID: 7782323
15. 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. PMID: 7665584
16. Wendel HG, Silva RL, Malina A, Mills JR, Zhu H, et al. (2007) Dissecting eIF4E action in tumorigenesis. Genes Dev 21: 3232-3237. PMID: 18055695
17. Furic L, Rong L, Larsson O, Koumakpayi IH, Yoshida K, et al. (2010) eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression. Proc Natl Acad Sci U S A 107: 14134-14139. doi: 10.1073/pnas.1005320107 PMID: 20679199
18. 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. PMID: 12423333
19. Slepenkov SV, Darzynkiewicz E, Rhoads RE (2006) Stopped-flow kinetic analysis of eIF4E and phosphorylated eIF4E binding to cap analogs and capped oligoribonucleotides: evidence for a one-step binding mechanism. J Biol Chem 281: 14927-14938. PMID: 16540463
20. Wendel HG, De Stanchina E, Fridman JS, Malina A, Ray S, et al. (2004) Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 428: 332-337. PMID: 15029198
21. Ruggero D, Montanaro L, Ma L, Xu W, Londei P, et al. (2004) The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat Med 10: 484-486. PMID: 15098029
22. 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. PMID: 15574771
23. McInerney GM, Kedersha NL, Kaufman RJ, Anderson P, Liljestrom P (2005) Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol Biol Cell 16: 3753-3763. PMID: 15930128
24. Anderson P, Kedersha N (2006) RNA granules. J Cell Biol 172: 803-808. PMID: 16520386
25. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, et al. (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169: 871-884. PMID: 15967811
26. Buchan JR, Muhlrad D, Parker R (2008) P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol 183: 441-455. doi: 10.1083/jcb.200807043 PMID: 18981231
27. Wang X, Yue P, Chan CB, Ye K, Ueda T, et al. (2007) Inhibition of mammalian target of rapamycin induces phosphatidylinositol 3-kinase-dependent and Mnk-mediated eukaryotic translation initiation factor 4E phosphorylation. Mol Cell Biol 27: 7405-7413. PMID: 17724079
28. Patel J, McLeod LE, Vries RG, Flynn A, Wang X, et al. (2002) Cellular stresses profoundly inhibit protein synthesis and modulate the states of phosphorylation of multiple translation factors. Eur J Biochem 269: 3076-3085. PMID: 12071973
29. Robichaud N, Del Rincon SV, Huor B, Alain T, Petruccelli LA, et al. Phosphorylation of eIF4E promotes EMT and metastasis via translational control of SNAIL and MMP-3. Oncogene.
30. Topisirovic I, Siddiqui N, Orolicki S, Skrabanek LA, Tremblay M, et al. (2009) Stability of eukaryotic translation initiation factor 4E mRNA is regulated by HuR, and this activity is dysregulated in cancer. Mol Cell Biol 29: 1152-1162. doi: 10.1128/MCB.01532-08 PMID: 19114552
31. Chen YC, Lin-Shiau SY, Lin JK (1998) Involvement of reactive oxygen species and caspase 3 activation in arsenite-induced apoptosis. J Cell Physiol 177: 324-333. PMID: 9766529
32. Wheater MJ, Johnson PW, Blaydes JP (2010) The role of MNK proteins and eIF4E phosphorylation in breast cancer cell proliferation and survival. Cancer Biol Ther 10: 728-735. doi: 10.4161/cbt.10.7.12965 PMID: 20686366
33. Dostie J, Lejbkowicz F, Sonenberg N (2000) Nuclear eukaryotic initiation factor 4E (eIF4E) colocalizes with splicing factors in speckles. J Cell Biol 148: 239-247. PMID: 10648556
34. Cargnello M, Tcherkezian J, Dorn JF, Huttlin EL, Maddox PS, et al. (2012) Phosphorylation of the eukaryotic translation initiation factor 4E-transporter (4E-T) by c-Jun N-terminal kinase promotes stressdependent P-body assembly. Mol Cell Biol 32: 4572-4584. doi: 10.1128/MCB.00544-12 PMID: 22966201
35. Clemens MJ, Bommer UA (1999) Translational control: the cancer connection. Int J Biochem Cell Biol 31: 1-23. PMID: 10216939
36. Rojo F, Najera L, Lirola J, Jimenez J, Guzman M, et al. (2007) 4E-binding protein 1, a cell signaling hallmark in breast cancer that correlates with pathologic grade and prognosis. Clin Cancer Res 13: 81-89. PMID: 17200342
37. Pons B, Peg V, Vazquez-Sanchez MA, Lopez-Vicente L, Argelaguet E, et al. (2011) The effect of p-4E-BP1 and p-eIF4E on cell proliferation in a breast cancer model. International journal of oncology 39: 1337-1345. doi: 10.3892/ijo.2011.1118 PMID: 21750861
38. Bilanges B, Stokoe D (2007) Mechanisms of translational deregulation in human tumors and therapeutic intervention strategies. Oncogene 26: 5973-5990. PMID: 17404576
39. Castellvi J, Garcia A, Rojo F, Ruiz-Marcellan C, Gil A, et al. (2006) Phosphorylated 4E binding protein 1: a hallmark of cell signaling that correlates with survival in ovarian cancer. Cancer 107: 1801-1811. PMID: 16983702
40. Armengol G, Rojo F, Castellvi J, Iglesias C, Cuatrecasas M, et al. (2007) 4E-binding protein 1: a key molecular "funnel factor" in human cancer with clinical implications. Cancer Res 67: 7551-7555. PMID: 17699757
41. Zhou FF, Yan M, Guo GF, Wang F, Qiu HJ, et al. (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. doi: 10.1007/s12032-010-9630-0 PMID: 20652449
42. Kubacka D, Kamenska A, Broomhead H, Minshall N, Darzynkiewicz E, et al. (2013) Investigating the consequences of eIF4E2 (4EHP) interaction with 4E-transporter on its cellular distribution in HeLa cells. PLoS One 8: e72761. doi: 10.1371/journal.pone.0072761 PMID: 23991149
43. Duncan RF, Peterson H, Hagedorn CH, Sevanian A (2003) Oxidative stress increases eukaryotic initiation factor 4E phosphorylation in vascular cells. Biochem J 369: 213-225. PMID: 12215171
44. Dong K, Wang R, Wang X, Lin F, Shen JJ, et al. (2009) Tumor-specific RNAi targeting eIF4E suppresses tumor growth, induces apoptosis and enhances cisplatin cytotoxicity in human breast carcinoma cells. Breast Cancer Res Treat 113: 443-456. doi: 10.1007/s10549-008-9956-x PMID: 18327707
45. Fraser CS, Pain VM, Morley SJ (1999) Cellular stress in xenopus kidney cells enhances the phosphorylation of eukaryotic translation initiation factor (eIF)4E and the association of eIF4F with poly(A)-binding protein. Biochem J 342 Pt 3: 519-526. PMID: 10477262
46. Walsh D, Mohr I (2004) Phosphorylation of eIF4E by Mnk-1 enhances HSV-1 translation and replication in quiescent cells. Genes Dev 18: 660-672. PMID: 15075293
47. Chen YJ, Tan BC, Cheng YY, Chen JS, Lee SC (2010) Differential regulation of CHOP translation by phosphorylated eIF4E under stress conditions. Nucleic Acids Res 38: 764-777. doi: 10.1093/nar/gkp1034 PMID: 19934253
48. Herdy B, Jaramillo M, Svitkin YV, Rosenfeld AB, Kobayashi M, et al. (2012) Translational control of the activation of transcription factor NF-kappaB and production of type I interferon by phosphorylation of the translation factor eIF4E. Nat Immunol 13: 543-550. doi: 10.1038/ni.2291 PMID: 22544393
49. Avdulov S, Li S, Michalek V, Burrichter D, Peterson M, et al. (2004) Activation of translation complex eIF4F is essential for the genesis and maintenance of the malignant phenotype in human mammary epithelial cells. Cancer Cell 5: 553-563. PMID: 15193258
50. Hong DS, Kurzrock R, Oh Y, Wheler J, Naing A, et al. (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. doi: 10.1158/1078-0432.CCR-11-0430 PMID: 21831956
51. Moerke NJ, Aktas H, Chen H, Cantel S, Reibarkh MY, et al. (2007) Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128: 257-267. PMID: 17254965
52. Volpon L, Osborne MJ, Zahreddine H, Romeo AA, Borden KL (2013) Conformational changes induced in the eukaryotic translation initiation factor eIF4E by a clinically relevant inhibitor, ribavirin triphosphate. Biochem Biophys Res Commun 434: 614-619. doi: 10.1016/j.bbrc.2013.03.125 PMID: 23583375
53. Konicek BW, Stephens JR, McNulty AM, Robichaud N, Peery RB, 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. doi: 10.1158/0008-5472.CAN-10-3298 PMID: 21233335
54. Stead RL, Proud CG (2013) Rapamycin enhances eIF4E phosphorylation by activating MAP kinase-interacting kinase 2a (Mnk2a). FEBS Lett 587: 2623-2628. doi: 10.1016/j.febslet.2013.06.045 PMID: 23831578
55. 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. PMID: 15254222
56. Aasen T, Belmonte JC (2010) Isolation and cultivation of human keratinocytes from skin or plucked hair for the generation of induced pluripotent stem cells. Nat Protoc 5: 371-382. doi: 10.1038/nprot.2009.241 PMID: 20134422