Pancreatic tumours escape from translational control through 4E-BP1 loss

Oncogene

Volumn 33, Issue 11, 2014, Pages 1367-1374

  Martineau, Y ^a   Azar, R ^a,b   Muller D ^a   Lasfargues, C ^a   El Khawand, S ^a   Anesia, R ^a   Pelletier, J ^c   Bousquet, C ^a   Pyronnet, S ^a,d  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b LEBANESE UNIVERSITY   (Lebanon)

^c MCGILL UNIVERSITY   (Canada)

^d CHU RANGUEIL   (France)

Author keywords

4E BP1; eIF4E phosphorylation; pancreatic cancer; translation initiation

Indexed keywords

CAP BINDING PROTEIN; EIF4E BINDING PROTEIN 1; INITIATION FACTOR 4E; K RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL PROLIFERATION; CELL TRANSFORMATION; GENE MUTATION; GENETIC MODEL; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; ONCOGENE K RAS; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION;

EUKARYOTA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CARCINOGENESIS; HUMANS; PANCREATIC NEOPLASMS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS;

EID: 84896401907     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.100     Document Type: Article

References (32)

1. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009; 136: 731-745.
2. Blagden SP, Willis AE. The biological and therapeutic relevance of mRNA translation in cancer. Nat Rev Clin Oncol 2011; 8: 280-291.
3. Waskiewicz AJ, Johnson JC, Penn B, Mahalingam M, Kimball SR, Cooper JA. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol Cell Biol 1999; 19: 1871-1880. (Pubitemid 29098245)
4. Pyronnet S, Imataka H, Gingras AC, Fukunaga R, Hunter T, Sonenberg N. Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. EMBO J 1999; 18: 270-279. (Pubitemid 29005042)
5. Furic L, Rong L, Larsson O, Koumakpayi IH, Yoshida K, Brueschke A et al. eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression. Proc Natl Acad Sci USA 2010; 107: 14134-14139.
6. Ueda T, Sasaki M, Elia AJ, Chio II, Hamada K, Fukunaga R et al. Combined deficiency for MAP kinase-interacting kinase 1 and 2 (Mnk1 and Mnk2) delays tumor development. Proc Natl Acad Sci USA 2010; 107: 13984-13990.
7. Martineau Y, Azar R, Bousquet C, Pyronnet S. Anti-oncogenic potential of the eIF4E-binding proteins. Oncogene 2013; 32: 671-677.
8. Wander SA, Hennessy BT, Slingerland JM. Next-generation mTOR inhibitors in clinical oncology: how pathway complexity informs therapeutic strategy. J Clin Invest 2011; 121: 1231-1241.
9. Wolpin BM, Hezel AF, Abrams T, Blaszkowsky LS, Meyerhardt JA, Chan JA et al. Oral mTOR inhibitor everolimus in patients with gemcitabine-refractory meta-static pancreatic cancer. J Clin Oncol 2009; 27: 193-198.
10. Hidalgo M. Pancreatic cancer. N Engl J Med 2010; 362: 1605-1617.
11. Bragado MJ, Tashiro M, Williams JA. Regulation of the initiation of pancreatic digestive enzyme protein synthesis by cholecystokinin in rat pancreas in vivo. Gastroenterology 2000; 119: 1731-1739. (Pubitemid 32198698)
12. Sans MD, Tashiro M, Vogel NL, Kimball SR, D'Alecy LG, Williams JA. Leucine activates pancreatic translational machinery in rats and mice through mTOR independently of CCK and insulin. J Nutr 2006; 136: 1792-1799. (Pubitemid 43973578)
13. Tsukiyama-Kohara K, Poulin F, Kohara M, DeMaria CT, Cheng A, Wu Z et al. Adipose tissue reduction in mice lacking the translational inhibitor 4E-BP1. Nat Med 2001; 7: 1128-1132. (Pubitemid 33010021)
14. Tsukiyama-Kohara K, Vidal SM, Gingras AC, Glover TW, Hanash SM, Heng H et al. Tissue distribution, genomic structure, and chromosome mapping of mouse and human eukaryotic initiation factor 4E-binding proteins 1 and 2. Genomics 1996; 38: 353-363. (Pubitemid 27030124)
15. Morris JPT, Wang SC, Hebrok M. KRAS, Hedgehog, Wnt and the twisted developmental biology of pancreatic ductal adenocarcinoma. Nat Rev Cancer 2010; 10: 683-695.
16. Pin CL, Rukstalis JM, Johnson C, Konieczny SF. The bHLH transcription factor Mist1 is required to maintain exocrine pancreas cell organization and acinar cell identity. J Cell Biol 2001; 155: 519-530. (Pubitemid 34289311)
17. Bidinosti M, Ran I, Sanchez-Carbente MR, Martineau Y, Gingras AC, Gkogkas C et al. Postnatal deamidation of 4E-BP2 in brain enhances its association with raptor and alters kinetics of excitatory synaptic transmission. Mol cell 2010; 37: 797-808.
18. Adesso L, Calabretta S, Barbagallo F, Capurso G, Pilozzi E, Geremia R et al. Gemcitabine triggers a pro-survival response in pancreatic cancer cells through activation of the MNK2/eIF4E pathway. Oncogene 2013; 32: 2848-2857.
19. Azar R, Alard A, Susini C, Bousquet C, Pyronnet S. 4E-BP1 is a target of Smad4 essential for TGFbeta-mediated inhibition of cell proliferation. EMBO J 2009; 28: 3514-3522.
20. Feldman ME, Apsel B, Uotila A, Loewith R, Knight ZA, Ruggero D et al. Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol 2009; 7: e38.
21. Schmidt EK, Clavarino G, Ceppi M, Pierre P. SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods 2009; 6: 275-277.
22. Averous J, Fonseca BD, Proud CG. Regulation of cyclin D1 expression by mTORC1 signaling requires eukaryotic initiation factor 4E-binding protein 1. Oncogene 2008; 27: 1106-1113. (Pubitemid 351253179)
23. Topisirovic I, Ruiz-Gutierrez M, Borden KL. Phosphorylation of the eukaryotic translation initiation factor eIF4E contributes to its transformation and mRNA transport activities. Cancer Res 2004; 64: 8639-8642. (Pubitemid 39552077)
24. Cencic R, Desforges M, Hall DR, Kozakov D, Du Y, Min J et al. Blocking eIF4E-eIF4G Interaction as a Strategy To Impair Coronavirus Replication. J Virol 2011; 85: 6381-6389.
25. Biankin AV, Waddell N, Kassahn KS, Gingras MC, Muthuswamy LB, Johns AL et al. Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 2012; 491: 399-405.
26. Armengol G, Rojo F, Castellvi J, Iglesias C, Cuatrecasas M, Pons B et al. 4E-binding protein 1: a key molecular 'funnel factor' in human cancer with clinical implications. Cancer Res 2007; 67: 7551-7555. (Pubitemid 47281345)
27. O'Reilly KE, Warycha M, Davies MA, Rodrik V, Zhou XK, Yee H et al. Phosphorylated 4E-BP1 is associated with poor survival in melanoma. Clin Cancer Res 2009; 15: 2872-2878.
28. Rojo F, Najera L, Lirola J, Jimenez J, Guzman M, Sabadell MD et al. 4E-binding protein 1, a cell signaling hallmark in breast cancer that correlates with pathologic grade and prognosis. Clin Cancer Res 2007; 13: 81-89. (Pubitemid 46121856)
29. Alain T, Morita M, Fonseca BD, Yanagiya A, Siddiqui N, Bhat M et al. eIF4E/4E-BP ratio predicts the efficacy of mTOR targeted therapies. Cancer Res 2012; 72: 6468-6476.
30. Cencic R, Hall DR, Robert F, Du Y, Min J, Li L et al. Reversing chemoresistance by small molecule inhibition of the translation initiation complex eIF4F. Proc Natl Acad Sci USA 2011; 108: 1046-1051.
31. Dowling RJ, Topisirovic I, Alain T, Bidinosti M, Fonseca BD, Petroulakis E et al. mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science (New York, NY) 2010; 328: 1172-1176.
32. Mamane Y, Petroulakis E, Martineau Y, Sato TA, Larsson O, Rajasekhar VK et al. Epigenetic activation of a subset of mRNAs by eIF4E explains its effects on cell proliferation. PLoS ONE 2007; 2: e242.