Mutational analysis of the DEAD-box RNA helicase eIF4AII characterizes its interaction with transformation suppressor Pdcd4 and eIF4GI

RNA

Volumn 11, Issue 3, 2005, Pages 261-274

  Zakowicz, Halina ^a,b   Yang, Hsin Sheng ^b   Stark, Cristi ^b,c   Wlodawer, Alexander ^b   Laronde Leblanc, Nicole ^b   Colburn, Nancy H ^b  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

EIF4A homology model; EIF4F; Translation initiation; Tumor suppressor

Indexed keywords

INITIATION FACTOR 4A; INITIATION FACTOR 4AII; INITIATION FACTOR 4G; INITIATION FACTOR 4G1; RNA HELICASE; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ANALYTIC METHOD; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL TRANSFORMATION; ENZYME ACTIVITY; GENE INACTIVATION; GENE MUTATION; GENETIC ANALYSIS; HYDROLYSIS; MOLECULAR INTERACTION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; TUMOR SUPPRESSOR GENE; TWO HYBRID SYSTEM; WILD TYPE;

AMINO ACID SEQUENCE; BASE SEQUENCE; DNA PRIMERS; EUKARYOTIC INITIATION FACTOR-4A; EUKARYOTIC INITIATION FACTOR-4G; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; PEPTIDE INITIATION FACTORS; POINT MUTATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS;

ANIMALIA; EUKARYOTA;

EID: 13944274057     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.7191905     Document Type: Article

References (34)

1. Afonja, O., Juste, D., Das, S., Matsuhashi, S., and Samuels, H.H. 2004. Induction of PDCD4 tumor suppressor gene expression by RAR agonists, antiestrogen and HER-2/neu antagonist in breast cancer cells. Evidence for a role in apoptosis. Oncogene 23: 8135-8145.
2. Aravind, L. and Koonin, E.V. 2000. Eukaryote-specific domains in translation initiation factors: Implications for translation regulation and evolution of the translation system. Genome Res. 10: 1172-1184.
3. Caruthers, J.M., Johnson, E.R., and McKay, D.B. 2000. Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. Proc. Natl. Acad. Sci. 97: 13080-13085.
4. Cmarik, J.L., Min, H., Hegamyer, G., Zhan, S., Kulesz-Martin, M., Yoshinaga, H., Matsuhashi, S., and Colburn, N.H. 1999. Differentially expressed protein Pdcd4 inhibits tumor promoter-induced neoplastic transformation. Proc. Natl. Acad. Sci. 96: 14037-14042.
5. De Gregorio, E., Preiss, T., and Hentze, M.W. 1998. Translational activation of uncapped mRNAs by the central part of human eIF4G is 5′ end-dependent. RNA 4: 828-836.
6. Waf1/Cip1. Am. J. Physiol. Cell Physiol. 287: C1541-C1546.
7. Guex, N. and Peitsch, M.C. 1997. SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
8. Imataka, H. and Sonenberg, N. 1997. Human eukaryotic translation initiation factor 4G (eIF4G) possesses two separate and independent binding sites for eIF4A. Mol. Cell. Biol. 17: 6940-6947.
9. Korneeva, N.L., Lamphear, B.J., Hennigan, F.L., and Rhoads, R.E. 2000. Mutually cooperative binding of eukaryotic translation initiation factor (eIF) 3 and eIF4A to human eIF4G-1. J. Biol. Chem. 275: 41369-41376.
10. Korneeva, N.L., Lamphear, B.J., Hennigan, F.L., Merrick, W.C., and Rhoads, R.E. 2001. Characterization of the two eIF4A-binding sites on human eIF4G-1. J. Biol. Chem. 276: 2872-2879.
11. Kressler, D., de la Cruz, J., Rojo, M., and Linder, P. 1997. Fal1p is an essential DEAD-box protein involved in 40S-ribosomal-subunit biogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 17: 7283-7294.
12. Li, W., Belsham, G.J., and Proud, G.G. 2001. Eukaryotic initiation factors 4A (eIF4A) and 4G (eIF4G) mutually interact in a 1:1 ratio in vivo. J. Biol. Chem. 276: 29111-29115.
13. Linder, P. 2003. Yeast RNA helicases of the DEAD-box family involved in translation initiation. Biol. Cell 95: 157-167.
14. Linder, P., Lasko, P.F., Ashburner, M., Leroy, P., Nielsen, P.J., Nishi, K., Schnier, J., and Slonimski, P.P. 1989. Birth of the D-E-A-D box. Nature 337: 121-122.
15. Lomakin, I.B., Hellen, C.U., and Pestova, T.V. 2000. Physical association of eukaryotic initiation factor 4G (eIF4G) with eIF4A strongly enhances binding of eIF4G to the internal ribosomal entry site of encephalomyocarditis virus and is required for internal initiation of translation. Mol. Cell. Biol. 20: 6019-6029.
16. Morino, S., Imataka, H., Svitkin, Y.V., Pestova, T.V., and Sonenberg, N. 2000. Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region. Mol. Cell. Biol. 20: 468-477.
17. Pain, V.M. 1996. Initiation of protein synthesis in eukaryotic cells. Eur. J. Biochem. 236: 747-771.
18. Pause, A. and Sonenberg, N. 1992. Mutational analysis of a DEAD box RNA helicase: The mammalian translation initiation factor eIF-4A. EMBO J. 11: 2643-2654.
19. Pause, A., Methot, N., and Sonenberg, N. 1993. The HRIGRXXR region of the DEAD box RNA helicase eukaryotic translation initiation factor 4A is required for RNA binding and ATP hydrolysis. Mol. Cell. Biol. 13: 6789-6798.
20. Pause, A., Methot, N., Svitkin, Y., Merrick, W.C., and 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.
21. Polunovsky, V.A., Gingras, A.C., Sonenberg, N., Peterson, M., Tan, A., Rubins, J.B., Manivel, J.C., and Bitterman, P.B. 2000. Translational control of the antiapoptotic function of Ras. J. Biol. Chem. 275: 24776-24780.
22. Ponting, C.P. 2000. Novel eIF4G domain homologues linking mRNA translation with nonsense-mediated mRNA decay. Trends Biochem. Sci. 25: 423-426.
23. Ray, B.K., Lawson, T.G., Kramer, J.C., Cladaras, M.H., Grifo, J.A., Abramson, R.D., Merrick, W.C., and Thach, R.E. 1985. ATP-dependent unwinding of messenger RNA structure by eukaryotic initiation factors. J. Biol. Chem. 260: 7651-7658.
24. Rocak, S. and Linder, P. 2004. DEAD-box proteins: The driving forces behind RNA metabolism. Nat. Rev. Mol. Cell. Biol. 5: 232-241.
25. Rogers Jr., G.W., Richter, N.J., and Merrick W.C. 1999. Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J. Biol. Chem. 274: 12236-12244.
26. Rogers Jr., G.W., Richter, N.J., Lima, W.F., and Merrick, W.C. 2001. Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. J. Biol. Chem. 276: 30914-30922.
27. Rozen, F., Edery, I., Meerovitch, K., Dever, T.E., Merrick, W.C., and Sonenberg, N. 1990. Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol. Cell. Biol. 10: 1134-1144.
28. Svitkin, Y.V., Pause, A., Haghighat, A., Pyronnet, S., Witherell, G., Belsham, G.J., and Sonenberg, N. 2001. The requirement for eukaryotic initiation factor 4A (eIF4A) in translation is in direct proportion to the degree of mRNA 5′ secondary structure. RNA 7: 382-394.
29. Tanner, N.K. and Linder, P. 2001. DExD/H box RNA helicases: From generic motors to specific dissociation functions. Mol. Cell 8: 251-262.
30. Tanner, N.K., Cordin, O., Banroques, J., Doere, M., and Linder, P. 2003. The Q motif: A newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol. Cell 11: 127-138.
31. Yang, H.-S., Jansen, A.P., Nair, R., Shibara, K., Verma, A.K., Cmarik, J.L., and Colburn, N.H. 2001. A novel transformation suppressor, Pdcd4, inhibits AP-1 transactivation but not NF-κB or ODC transactivation. Oncogene 20: 669-676.
32. Yang, H.S., Jansen, A.P., Komar, A.A., Zheng, X., Merrick, W.C., Costes, S., Lockett, S.J., Sonenberg, N., and Colburn, N.H. 2003a. The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol. Cell. Biol. 23: 26-37.
33. Yang, H.S., Knies, J.L., Stark, C., and Colburn, N.H. 2003b. Pdcd4 suppresses tumor phenotype in JB6 cells by inhibiting AP-1 transactivation. Oncogene 22: 3712-3720.
34. Yang, H.S., Cho, M.H., Zakowicz, H., Hegamyer, G., Sonenberg, N., and Colburn, N.H. 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.