Human eIF4E promotes mRNA restructuring by stimulating eIF4A helicase activity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 33, 2013, Pages 13339-13344

  Feoktistova, Kateryna ^a   Tuvshintogs, Enkhee ^a   Do, Angelie ^a   Fraser, Christopher S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ATPase; DEAD box; Protein synthesis

Indexed keywords

HELICASE; INITIATION FACTOR 4A; INITIATION FACTOR 4E; MESSENGER RNA;

5' UNTRANSLATED REGION; ARTICLE; BINDING AFFINITY; BINDING SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RIBOSOME; TRANSLATION INITIATION;

ATPASE; DEAD-BOX; PROTEIN SYNTHESIS;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CHROMATOGRAPHY, GEL; CHROMATOGRAPHY, ION EXCHANGE; ENZYME ACTIVATION; EUKARYOTIC INITIATION FACTOR-4A; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4G; HUMANS; OLIGONUCLEOTIDES; RNA, MESSENGER; SF9 CELLS; SPODOPTERA;

EID: 84882291342     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1303781110     Document Type: Article

References (45)

1. Ruggero D (2013) Translational control in cancer etiology. Cold Spring Harb Perspect Biol 5(2):a012336.
2. Silvera D, Formenti SC, Schneider RJ (2010) Translational control in cancer. Nat Rev Cancer 10(4):254-266.
3. 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.
4. 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(1):380-388.
5. Richter JD, Sonenberg N (2005) Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433(7025):477-480.
6. Pause A, et al. (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371(6500):762-767.
7. Hay N, Sonenberg N (2004) Upstream and downstream of mTOR. Genes Dev 18(16): 1926-1945.
8. Dowling RJ, et al. (2010) mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328(5982):1172-1176.
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(6275):544-547.
10. 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 USA 87(21):8212-8216.
11. Koromilas AE, Lazaris-Karatzas A, Sonenberg N (1992) mRNAs containing extensive secondary structure in their 5′ non-coding region translate efficiently in cells overexpressing initiation factor eIF-4E. EMBO J 11(11):4153-4158.
12. Ruggero D, et al. (2004) The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat Med 10(5):484-486.
13. Bordeleau ME, et al. (2006) Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat Chem Biol 2(4):213-220.
14. Svitkin YV, et al. (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(3):382-394.
15. Rogers GW, Jr., Richter NJ, Lima WF, Merrick WC (2001) Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. J Biol Chem 276(33):30914-30922.
16. Rogers GW, Jr., Richter NJ, Merrick WC (1999) Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J Biol Chem 274(18):12236-12244.
17. Rozen F, et al. (1990) Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol Cell Biol 10(3):1134-1144.
18. Hilbert M, Kebbel F, Gubaev A, Klostermeier D (2011) eIF4G stimulates the activity of the DEAD box protein eIF4A by a conformational guidance mechanism. Nucleic Acids Res 39(6):2260-2270.
19. Lorsch JR, Herschlag D (1998) The DEAD box protein eIF4A.
20. A cycle of nucleotide and RNA-dependent conformational changes. Biochemistry 37(8):2194-2206.
21. Marintchev A, et al. (2009) Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 136(3):447-460.
22. Özeş AR, Feoktistova K, Avanzino BC, Fraser CS (2011) Duplex unwinding and ATPase activities of the DEAD-box helicase eIF4A are coupled by eIF4G and eIF4B. J Mol Biol 412(4):674-687.
23. Korneeva NL, First EA, Benoit CA, Rhoads RE (2005) Interaction between the NH2- terminal domain of eIF4A and the central domain of eIF4G modulates RNA-stimulated ATPase activity. J Biol Chem 280(3):1872-1881.
24. Abramson RD, Dever TE, Merrick WC (1988) Biochemical evidence supporting a mechanism for cap-independent and internal initiation of eukaryotic mRNA. J Biol Chem 263(13):6016-6019.
25. Bi X, Ren J, Goss DJ (2000) Wheat germ translation initiation factor eIF4B affects eIF4A and eIFiso4F helicase activity by increasing the ATP binding affinity of eIF4A. Biochemistry 39(19):5758-5765.
26. Bi X, Goss DJ (2000) Wheat germ poly(A)-binding protein increases the ATPase and the RNA helicase activity of translation initiation factors eIF4A, eIF4B, and eIF-iso4F. J Biol Chem 275(23):17740-17746.
27. Zuberek J, et al. (2004) Influence of electric charge variation at residues 209 and 159 on the interaction of eIF4E with the mRNA 5′ terminus. Biochemistry 43(18):5370-5379.
28. Slepenkov SV, Korneeva NL, Rhoads RE (2008) Kinetic mechanism for assembly of the m7GpppG.eIF4E.eIF4G complex. J Biol Chem 283(37):25227-25237.
29. De Gregorio E, Preiss T, Hentze MW (1999) Translation driven by an eIF4G core domain in vivo. EMBO J 18(17):4865-4874.
30. Scheper GC, et al. (2002) Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affinity for capped mRNA. J Biol Chem 277(5):3303-3309.
31. 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 USA 93(3):1065-1070.
32. Graff JR, Konicek BW, Carter JH, Marcusson EG (2008) Targeting the eukaryotic translation initiation factor 4E for cancer therapy. Cancer Res 68(3):631-634.
33. Hiremath LS, Webb NR, Rhoads RE (1985) Immunological detection of the messenger RNA cap-binding protein. J Biol Chem 260(13):7843-7849.
34. Rau M, Ohlmann T, Morley SJ, Pain VM (1996) A reevaluation of the cap-binding protein, eIF4E, as a rate-limiting factor for initiation of translation in reticulocyte lysate. J Biol Chem 271(15):8983-8990.
35. Ohlmann T, Pain VM, Wood W, Rau M, Morley SJ (1997) The proteolytic cleavage of eukaryotic initiation factor (eIF) 4G is prevented by eIF4E binding protein (PHAS-I; 4EBP1) in the reticulocyte lysate. EMBO J 16(4):844-855.
36. Haghighat A, et al. (1996) The eIF4G-eIF4E complex is the target for direct cleavage by the rhinovirus 2A proteinase. J Virol 70(12):8444-8450.
37. Gross JD, et al. (2003) Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115(6):739-750.
38. Ohlmann T, Rau M, Pain VM, Morley SJ (1996) The C-terminal domain of eukaryotic protein synthesis initiation factor (eIF) 4G is sufficient to support cap-independent translation in the absence of eIF4E. EMBO J 15(6):1371-1382.
39. Thoreen CC, et al. (2012) A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485(7396):109-113.
40. Hsieh AC, et al. (2012) The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 485(7396):55-61.
41. Damgaard CK, Lykke-Andersen J (2011) Translational coregulation of 5'TOP mRNAs by TIA-1 and TIAR. Genes Dev 25(19):2057-2068.
42. Shama S, Avni D, Frederickson RM, Sonenberg N, Meyuhas O (1995) Overexpression of initiation factor eIF-4E does not relieve the translational repression of ribosomal protein mRNAs in quiescent cells. Gene Expr 4(4-5):241-252.
43. Alain T, et al. (2012) eIF4E/4E-BP ratio predicts the efficacy of mTOR targeted therapies. Cancer Res 72(24):6468-6476.
44. Fraser CS, Berry KE, Hershey JW, Doudna JA (2007) eIF3j is located in the decoding center of the human 40S ribosomal subunit. Mol Cell 26(6):811-819.
45. Siridechadilok B, Fraser CS, Hall RJ, Doudna JA, Nogales E (2005) Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310(5753):1513-1515.