Multiple elements in the eIF4G1 N-terminus promote assembly of eIF4G1•PABP mRNPs in vivo

EMBO Journal

Volumn 30, Issue 2, 2011, Pages 302-316

  Park, Eun Hee ^a   Walker, Sarah E ^b   Lee, Joseph M ^c   Rothenburg, Stefan ^a   Lorsch, Jon R ^b   Hinnebusch, Alan G ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

eIF4G; initiation; PABP; translation; yeast

Indexed keywords

FUNGAL PROTEIN; INITIATION FACTOR 4G; POLYADENYLIC ACID BINDING PROTEIN; PROTEIN BOX1; PROTEIN BOX2; PROTEIN EIF4G1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; RNA BINDING;

AMINO ACID SEQUENCE; BASE SEQUENCE; EUKARYOTIC INITIATION FACTOR-4G; FLUORESCENCE POLARIZATION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; POLY(A)-BINDING PROTEINS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RIBONUCLEOPROTEINS; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 78751609906     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.312     Document Type: Article

References (42)

1. Altmann M, Sonenberg N, Trachsel H (1989) Translation in Saccharomyces cerevisiae: initiation factor 4E-dependent cell-free system. Mol Cell Biol 9: 4467-4472 (Pubitemid 19239616)
2. Amrani N, Ghosh S, Mangus DA, Jacobson A (2008) Translation factors promote the formation of two states of the closed-loop mRNP. Nature 453: 1276-1280
3. Berset C, Zurbriggen A, Djafarzadeh S, Altmann M, Trachsel H (2003) RNA-binding activity of translation initiation factor eIF4G1 from Saccharomyces cerevisiae. RNA 9: 871-880
4. Clarkson BK, Gilbert WV, Doudna JA (2010) Functional overlap between eIF4G isoforms in Saccharomyces cerevisiae. PLoS One 5: e9114
5. de la Cruz J, Iost I, Kressler D, Linder P (1997) The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 94: 5201-5206
6. Deardorff JA, Sachs AB (1997) Differential effects of aromatic and charged residue substitutions in the RNA binding domains of the yeast poly(A)-binding protein. J Mol Biol 269: 67-81
7. Dominguez D, Altmann M, Benz J, Baumann U, Trachsel H (1999) Interaction of translation initiation factor eIF4G with eIF4A in the yeast Saccharomyces cerevisiae. J Biol Chem 274: 26720-26726
8. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425: 737-741
9. Goyer C, Altmann M, Lee HS, Blanc A, Deshmukh M, Woolford JL, Trachsel H, Sonenberg N (1993) TIF4631 and TIF4632: Two yeast genes encoding the high-molecular-weight subunits of the capbinding protein complex (eukaryotic initiation factor 4F) contain an RNA recognition motif-like sequence and carry out an essential function. Mol Cell Biol 13: 4860-4874
10. Goyer C, Altmann M, Trachsel H, Sonenberg N (1989) Identification and characterization of cap binding proteins from yeast. J Biol Chem 264: 7603-7610
11. Groft CM, Burley SK (2002) Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Mol Cell 9: 1273-1283
12. Guthrie C, Fink G (1991) Guide to yeast genetics and molecular biology. Methods Enzymol 194: 1-863
13. He H, von der Haar T, Singh CR, Ii M, Li B, Hinnebusch AG, McCarthy JE, Asano K (2003) The yeast eukaryotic initiation factor 4G (eIF4G) HEAT domain interacts with eIF1 and eIF5 and is involved in stringent AUG selection. Mol Cell Biol 23: 5431-5445
14. Hinton TM, Coldwell MJ, Carpenter GA, Morley SJ, Pain VM (2007) Functional analysis of individual binding activities of the scaffold protein eIF4G. J Biol Chem 282: 1695-1708
15. Imataka H, Gradi A, Sonenberg N (1998) A newly identified N-terminal amino acid sequence of human eIF4G binds poly (A)-binding protein and functions in poly(A)-dependent translation. EMBO J 17: 7480-7489
16. Kahvejian A, Svitkin YV, Sukarieh R, M'Boutchou MN, Sonenberg N (2005) Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev 19: 104-113
17. Kaye NM, Emmett KJ, Merrick WC, Jankowsky E (2009) Intrinsic RNA binding by the eukaryotic initiation factor 4F depends on a minimal RNA length but not on the m7G cap. J Biol Chem 284: 17742-17750
18. Kessler SH, Sachs AB (1998) RNA recognition motif 2 of yeast Pab1p is required for its functional interaction with eukaryotic translation initiation factor 4G. Mol Cell Biol 18: 51-57
19. Khaleghpour K, Svitkin YV, Craig AW, DeMaria CT, Deo RC, Burley SK, Sonenberg N (2001) Translational repression by a novel partner of human poly(A) binding protein, Paip2. Mol Cell 7: 205-216
20. LeFebvre AK, Korneeva NL, Trutschl M, Cvek U, Duzan RD, Bradley CA, Hershey JW, Rhoads RE (2006) Translation initiation factor eIF4G-1 binds to eIF3 through the eIF3e subunit. J Biol Chem 281: 22917-22932
21. Maag D, Lorsch JR (2003) Communication between eukaryotic translation initiation factors 1 and 1A on the yeast small ribosomal subunit. J Mol Biol 330: 917-924
22. Michel YM, Poncet D, Piron M, Kean KM, Borman AM (2000) Cap-Poly(A) synergy in mammalian cell-free extracts. Investigation of the requirements for poly(A)-mediated stimulation of translation initiation. J Biol Chem 275: 32268-32276
23. Mitchell S, Walker S, Algire M, Park E-H, Hinnebusch A, Lorsch J (2010) The 50-7-methylguanosine cap on eukaryotic mRNAs serves both to stimulate canonical translation initiation and block an alternative pathway. Mol Cell 39: 950-962
24. Nanda JS, Cheung YN, Takacs JE, Martin-Marcos P, Saini AK, Hinnebusch AG, Lorsch JR (2009) eIF1 controls multiple steps in start codon recognition during eukaryotic translation initiation. J Mol Biol 394: 268-285
25. Neff CL, Sachs AB (1999) Eukaryotic translation initiation factors eIF4G and eIF4A from Saccharomyces cerevisiae physically and functionally interact. Mol Cell Biol 19: 5557-5564
26. Pestova TV, Kolupaeva VG (2002) The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev 16: 2906-2922
27. Poyry TA, Kaminski A, Jackson RJ (2004) What determines whether mammalian ribosomes resume scanning after translation of a short upstream open reading frame? Genes Dev 18: 62-75
28. Prevot D, Decimo D, Herbreteau CH, Roux F, Garin J, Darlix JL, Ohlmann T (2003) Characterization of a novel RNA-binding region of eIF4GI critical for ribosomal scanning. EMBO J 22: 1909-1921
29. Qiu H, Garcia-Barrio MT, Hinnebusch AG (1998) Dimerization by translation initiation factor 2 kinase GCN2 is mediated by interactions in the C-terminal ribosome-binding region and the protein kinase domain. Mol Cell Biol 18: 2697-2711
30. Reid GA, Schatz G (1982) Import of proteins into mitochondria. Yeast cells grown in the presence of carbonyl cyanide m-chlorophenylhydrazone accumulate massive amounts of some mitochondrial precursor polypeptides. J Biol Chem 257: 13056-13061
31. Sachs A (2000) Physical and functional interactions between the mRNA cap structure and the poly(A) tail. In Sonenberg N, Hershey JWB, Mathews MB (eds) Translational Control of Gene Expression, Sonenberg N, Hershey JWB, Mathews MB (eds) pp 447-465. Cold Spring Harbor: Cold Spring Harbor Laboratory Press
32. Sachs AB, Davis RW, Kornberg RD (1987) A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability. Mol Cell Biol 7: 3268-3276
33. Sonenberg N, Hinnebusch AG (2007) New modes of translational control in development, behavior, and disease. Mol Cell 28: 721-729
34. Svitkin YV, Evdokimova VM, Brasey A, Pestova TV, Fantus D, Yanagiya A, Imataka H, Skabkin MA, Ovchinnikov LP, Merrick WC, Sonenberg N (2009) General RNA-binding proteins have a function in poly(A)-binding protein-dependent translation. EMBO J 28: 58-68
35. Tarun Jr SZ, Sachs AB (1997) Binding of eukaryotic translation initiation factor 4E (eIF4E) to eIF4G represses translation of uncapped mRNA. Mol Cell Biol 17: 6876-6886
36. Tarun SZ, Sachs AB (1995) A common function for mRNA 50 and 30 ends in translation initiation in yeast. Genes Dev 9: 2997-3007
37. Tarun SZ, Sachs AB (1996) Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J 15: 7168-7177
38. Tarun SZ, Wells SE, Deardorff JA, Sachs AB (1997) Translation initiation factor eIF4G mediates in vitro poly (A) tail-dependent translation. Proc Natl Acad Sci USA 94: 9046-9051
39. von Der Haar T, Ball PD, McCarthy JE (2000) Stabilization of eukaryotic initiation factor 4E binding to the mRNA 50-Cap by domains of eIF4G. J Biol Chem 275: 30551-30555
40. von der Haar T, McCarthy JE (2002) Intracellular translation initiation factor levels in Saccharomyces cerevisiae and their role in cap-complex function. Mol Microbiol 46: 531-544
41. Wei CC, Balasta ML, Ren J, Goss DJ (1998) Wheat germ poly(A) binding protein enhances the binding affinity of eukaryotic initiation factor 4F and (iso)4F for cap analogues. Biochemistry 37: 1910-1916
42. Yanagiya A, Svitkin YV, Shibata S, Mikami S, Imataka H, Sonenberg N (2009) Requirement of RNA binding of mammalian eukaryotic translation initiation factor 4GI (eIF4GI) for efficient interaction of eIF4E with the mRNA cap. Mol Cell Biol 29: 1661-1669