L13a Blocks 48S Assembly: Role of a General Initiation Factor in mRNA-Specific Translational Control

Molecular Cell

Volumn 25, Issue 1, 2007, Pages 113-126

  Kapasi, Purvi ^a   Chaudhuri, Sujan ^a   Vyas, Keyur ^a   Baus, Diane ^b   Komar, Anton A ^a   Fox, Paul L ^a,c   Merrick, William C ^b   Mazumder, Barsanjit ^a  

^a CLEVELAND STATE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

RNA

Indexed keywords

CASPASE; CERULOPLASMIN; GAMMA INTERFERON; GAMMA INTERFERON ACTIVATED INHIBITOR OF TRANSLATION COMPLEX PROTEIN; HYBRID PROTEIN; INITIATION FACTOR 4F; INITIATION FACTOR 4G; MESSENGER RNA; PROTEIN L13A; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; COMPLEX FORMATION; GENE EXPRESSION; GENE SILENCING; HUMAN; INTERNAL RIBOSOME ENTRY SITE; MACROPHAGE; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; PROTEIN TARGETING; RIBOSOME SUBUNIT; RNA TRANSLATION; TRANSLATION INITIATION; TRANSLATION REGULATION;

BINDING SITES; EUKARYOTIC INITIATION FACTOR-3; EUKARYOTIC INITIATION FACTOR-4F; EUKARYOTIC INITIATION FACTOR-4G; GENE EXPRESSION REGULATION; GENES, REPORTER; MODELS, GENETIC; PEPTIDE INITIATION FACTORS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, TERTIARY; REGULATORY SEQUENCES, NUCLEIC ACID; RIBOSOMAL PROTEINS; RIBOSOMES; RNA CAPS; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 33846004827     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.11.028     Document Type: Article

References (46)

1. Aragon T., de la Luna S., Novoa I., Carrasco L., Ortin J., and Nieto A. Eukaryotic translation initiation factor 4GI is a cellular target for NS1 protein, a translational activator of influenza virus. Mol. Cell. Biol. 20 (2000) 6259-6268
2. Beckmann K., Grskovic M., Gebauer F., and Hentze M.W. A dual inhibitory mechanism restricts msl-2 mRNA translation for dosage compensation in Drosophila. Cell 122 (2005) 529-540
3. Bergamini G., Preiss T., and Hentze M.W. Picornavirus IRESes and the poly(A) tail jointly promote cap-independent translation in a mammalian cell-free system. RNA 6 (2000) 1781-1790
4. Cho P.F., Poulin F., Cho-Park Y.A., Cho-Park I.B., Chicoine J.D., Lasko P., and Sonenberg N. A new paradigm for translational control: inhibition via 5′-3′ mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell 121 (2005) 411-423
5. Clemens M.J., Bushell M., and Morley S.J. Degradation of eukaryotic polypeptide chain initiation factor (eIF) 4G in response to induction of apoptosis in human lymphoma cell lines. Oncogene 17 (1998) 2921-2931
6. Cuesta R., Laroia G., and Schneider R.J. Chaperone hsp27 inhibits translation during heat shock by binding eIF4G and facilitating dissociation of cap-initiation complexes. Genes Dev. 14 (2000) 1460-1470
7. Cuesta R., Xi Q., and Schneider R.J. Structural basis for competitive inhibition of eIF4G-Mnk1 interaction by the adenovirus 100-kilodalton protein. J. Virol. 78 (2004) 7707-7716
8. Dever T.E. Gene-specific regulation by general translation factors. Cell 108 (2002) 545-556
9. Fox P.L., Mazumder B., Ehrenwald E., and Mukhopadhyay C.K. Ceruloplasmin and cardiovascular disease. Free Radic. Biol. Med. 28 (2000) 1735-1744
10. Gebauer F., and Hentze M.W. Molecular mechanisms of translational control. Nat. Rev. Mol. Cell Biol. 5 (2004) 827-835
11. Gebauer F., Grskovic M., and Hentze M.W. Drosophila sex-lethal inhibits the stable association of the 40S ribosomal subunit with msl-2 mRNA. Mol. Cell 11 (2003) 1397-1404
12. Gingras A.C., Raught B., and Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68 (1999) 913-963
13. Gray N.K., and Hentze M.W. Iron regulatory protein prevents binding of the 43S translation pre-initiation complex to ferritin and eALAS mRNAs. EMBO J. 13 (1994) 3882-3891
14. Jan E., and Sarnow P. Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J. Mol. Biol. 324 (2002) 889-902
15. Kolupaeva V.G., Lomakin I.B., Pestova T.V., and Hellen C.U. Eukaryotic initiation factors 4G and 4A mediate conformational changes downstream of the initiation codon of the encephalomyocarditis virus internal ribosomal entry site. Mol. Cell. Biol. 23 (2003) 687-698
16. LeFebvre A.K., Korneeva N.L., Trutschl M., Cvek U., Duzan R.D., Bradley C.A., Hershey J.W., and Rhoads R.E. Translation initiation factor eIF4G-1 binds to eIF3 through the eIF3e subunit. J. Biol. Chem. 281 (2006) 22917-22932
17. Marissen W.E., and Lloyd R.E. Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol. Cell. Biol. 18 (1998) 7565-7574
18. Mazumder B., and Fox P.L. Delayed translational silencing of ceruloplasmin transcript in gamma interferon-activated U937 monocytic cells: role of the 3′ untranslated region. Mol. Cell. Biol. 19 (1999) 6898-6905
19. Mazumder B., Mukhopadhyay C.K., Prok A., Cathcart M.K., and Fox P.L. Induction of ceruloplasmin synthesis by IFN-gamma in human monocytic cells. J. Immunol. 159 (1997) 1938-1944
20. Mazumder B., Seshadri V., Imataka H., Sonenberg N., and Fox P.L. Translational silencing of ceruloplasmin requires the essential elements of mRNA circularization: poly(A) tail, poly(A)-binding protein, and eukaryotic translation initiation factor 4G. Mol. Cell. Biol. 21 (2001) 6440-6449
21. Mazumder B., Sampath P., Seshadri V., Maitra R.K., DiCorleto P.E., and Fox P.L. Regulated release of L13a from the 60S ribosomal subunit as a mechanism of transcript-specific translational control. Cell 115 (2003) 187-198
22. Mazumder B., Seshadri V., and Fox P.L. Translational control by the 3′-UTR: the ends specify the means. Trends Biochem. Sci. 28 (2003) 91-98
23. Michel Y.M., Borman A.M., Paulous S., and Kean K.M. Eukaryotic initiation factor 4G-poly(A) binding protein interaction is required for poly(A) tail-mediated stimulation of picornavirus internal ribosome entry segment-driven translation but not for X-mediated stimulation of hepatitis C virus translation. Mol. Cell. Biol. 21 (2001) 4097-4109
24. Muckenthaler M., Gray N.K., and Hentze M.W. IRP-1 binding to ferritin mRNA prevents the recruitment of the small ribosomal subunit by the cap-binding complex eIF4F. Mol. Cell 2 (1998) 383-388
25. Mukhopadhyay C.K., Mazumder B., Lindley P.F., and Fox P.L. Identification of the prooxidant site of human ceruloplasmin: a model for oxidative damage by copper bound to protein surfaces. Proc. Natl. Acad. Sci. USA 94 (1997) 11546-11551
26. Niessing D., Blanke S., and Jackle H. Bicoid associates with the 5′-cap-bound complex of caudal mRNA and represses translation. Genes Dev. 16 (2002) 2576-2582
27. Ostareck D.H., Ostareck-Lederer A., Wilm M., Thiele B.J., Mann M., and Hentze M.W. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell 89 (1997) 597-606
28. Ostareck D.H., Ostareck-Lederer A., Shatsky I.N., and Hentze M.W. Lipoxygenase mRNA silencing in erythroid differentiation: the 3′UTR regulatory complex controls 60S ribosomal subunit joining. Cell 104 (2001) 281-290
29. Pestova T.V., and Hellen C.U. Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes Dev. 17 (2003) 181-186
30. Pestova T.V., Hellen C.U., and Shatsky I.N. Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol. Cell. Biol. 16 (1996) 6859-6869
31. Pestova T.V., Shatsky I.N., and Hellen C.U. Functional dissection of eukaryotic initiation factor 4F: the 4A subunit and the central domain of the 4G subunit are sufficient to mediate internal entry of 43S preinitiation complexes. Mol. Cell. Biol. 16 (1996) 6870-6878
32. Pestova T.V., Shatsky I.N., Fletcher S.P., Jackson R.J., and Hellen C.U. A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev. 12 (1998) 67-83
33. Pestova T.V., Lomakin I.B., and Hellen C.U. Position of the CrPV IRES on the 40S subunit and factor dependence of IRES/80S ribosome assembly. EMBO Rep. 5 (2004) 906-913
34. Piron M., Vende P., Cohen J., and Poncet D. Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J. 17 (1998) 5811-5821
35. Prevot D., Darlix J.L., and Ohlmann T. Conducting the initiation of protein synthesis: the role of eIF4G. Biol. Cell. 95 (2003) 141-156
36. Prevot D., Decimo D., Herbreteau C.H., Roux F., Garin J., Darlix J.L., and Ohlmann T. Characterization of a novel RNA-binding region of eIF4GI critical for ribosomal scanning. EMBO J. 22 (2003) 1909-1921
37. Richter J.D., and Sonenberg N. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433 (2005) 477-480
38. Sampath P., Mazumder B., Seshadri V., and Fox P.L. Transcript-selective translational silencing by gamma interferon is directed by a novel structural element in the ceruloplasmin mRNA 3′ untranslated region. Mol. Cell. Biol. 23 (2003) 1509-1519
39. Sampath P., Mazumder B., Seshadri V., Gerber C.A., Chavatte L., Kinter M., Ting S.M., Dignam J.D., Kim S., Driscoll D.M., and Fox P.L. Noncanonical function of glutamyl-prolyl-tRNA synthetase: gene-specific silencing of translation. Cell 119 (2004) 195-208
40. Siridechadilok B., Fraser C.S., Hall R.J., Doudna J.A., and Nogales E. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310 (2005) 1513-1515
41. Skern T., Hampölz B., Guarné A., Fita I., Bergmann E., Petersen J., and James M.N.G. Structure and function of picornavirus proteinases. In: Semler B., and Wimmer E. (Eds). Molecular Biology of Picornaviruses (2002), ASM Press, Washington, D.C. 199-212
42. Stebbins-Boaz B., Cao Q., de Moor C.H., Mendez R., and Richter J.D. Maskin is a CPEB-associated factor that transiently interacts with eIF-4E. Mol. Cell 4 (1999) 1017-1027
43. Stripecke R., Oliveira C.C., McCarthy J.E., and Hentze M.W. Proteins binding to 5′ untranslated region sites: a general mechanism for translational regulation of mRNAs in human and yeast cells. Mol. Cell. Biol. 14 (1994) 5898-5909
44. Svitkin Y.V., Imataka H., Khaleghpour K., Kahvejian A., Liebig H.D., and Sonenberg N. Poly(A)-binding protein interaction with eIF4G stimulates picornavirus IRES-dependent translation. RNA 7 (2001) 1743-1752
45. Wang B., Love T.M., Call M.E., Doench J.G., and Novina C.D. Recapitulation of short RNA-directed translational gene silencing in vitro. Mol. Cell 22 (2006) 553-560
46. Wilson J.E., Powell M.J., Hoover S.E., and Sarnow P. Naturally occurring dicistronic cricket paralysis virus RNA is regulated by two internal ribosome entry sites. Mol. Cell. Biol. 20 (2000) 4990-4999