Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms

Genes and Development

Volumn 19, Issue 1, 2005, Pages 104-113

  Kahvejian, Avak ^a   Svitkin, Yuri V ^a   Sukarieh, Rami ^a   M'Boutchou, Marie Noël ^a   Sonenberg, Nahum ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Eukaryotic initiation factor 4G (eIF4G); mRNA circularization; mRNA translation; Poly(A) binding protein (PABP); Ribosome binding

Indexed keywords

CELL EXTRACT; INITIATION FACTOR 2; INITIATION FACTOR 4E; INITIATION FACTOR 4G; POLYADENYLIC ACID BINDING PROTEIN;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; GENE MUTATION; MAMMAL CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN INTERACTION; RIBOSOME; RNA CAPPING; RNA TRANSLATION; TRANSLATION INITIATION;

ANIMALS; CELL EXTRACTS; EUKARYOTIC INITIATION FACTOR-4G; EUKARYOTIC INITIATION FACTORS; HUMANS; POLY(A)-BINDING PROTEIN I; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBOSOMES;

EUKARYOTA; MAMMALIA;

EID: 11844281461     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1262905     Document Type: Article

References (50)

1. Afonina, E., Neumann, M., and Pavlakis, G.N. 1997. Preferential binding of poly(A)-binding protein 1 to an inhibitory RNA element in the human immunodeficiency virus type 1 gag mRNA. J. Biol. Chem. 272: 2307-2311.
2. Bi, X. and Goss, D.J. 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: 17740-17746.
3. Byrd, M.P., Zamora, M., and Lloyd, R.E. 2002. Generation of multiple isoforms of eukaryotic translation initiation factor 4GI by use of alternate translation initiation codons. Mol. Cell. Biol. 22: 4499-4511.
4. Copeland, P.R. and Wormington, M. 2001. The mechanism and regulation of deadenylation: Identification and characterization of Xenopus PARN. RNA 7: 875-886.
5. Edery, I., Humbelin, M., Darveau, A., Lee, K.A., Milburn, S., Hershey, J.W., Trachsel, H., and Sonenberg, N. 1983. Involvement of eukaryotic initiation factor 4A in the cap recognition process. J. Biol. Chem. 258: 11398-11403.
6. Gallie, D.R. 1991. The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes & Dev. 5: 2108-2116.
7. _. 1998. A tale of two termini: A functional interaction between the termini of an mRNA is a prerequisite for efficient translation initiation. Gene 216: 1-11.
8. Gingras, A.-C., Raught, B., and Sonenberg, N. 1999. eIF4 initiation factors: Effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68: 913-963.
9. Gray, N.K. and Hentze, M.W. 1994. Iron regulatory protein prevents binding of the 43S translation pre-initiation complex to ferritin and eALAS mRNAs. EMBO J. 13: 3882-3891.
10. Gray, N.K., Coller, J.M., Dickson, K.S., and Wickens, M. 2000. Multiple portions of poly(A)-binding protein stimulate translation in vivo. EMBO J. 19: 4723-4733.
11. Groft, C.M. and Burley, S.K. 2002. Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Mol. Cell 9: 1273-1283.
12. Gross, J.D., Moerke, N.J., von der Haar, T., Lugovskoy, A.A., Sachs, A.B., McCarthy, J.E., and Wagner, G. 2003. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115: 739-750.
13. Grosset, C., Chen, C.Y., Xu, N., Sonenberg, N., Jacquemin-Sablon, H., and Shyu, A.B. 2000. A mechanism for translationally coupled mRNA turnover: Interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell 103: 29-40.
14. Haghighat, A. and Sonenberg, N. 1997. eIF4G dramatically enhances the binding of eIF4E to the mRNA 5′-cap structure. J. Biol. Chem. 272: 21677-21680.
15. Hershey, J.W.B. and Merrick, W.C. 2000. The pathway and mechanism of initiation of protein synthesis. In Translational control of gene expression (ed. M.B. Mathews), pp. 33-88. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
16. Iizuka, N., Najita, L., Franzusoff, A., and Sarnow, P. 1994. Cap-dependent and cap-independent translation by internal initiation of mRNAs in cell extracts prepared from Saccharomyces cerevisiae. Mol. Cell. Biol. 14: 7322-7330.
17. Imataka, H., Gradi, A., and 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.
18. Jacobson, A. 1996. Poly(A) metabolism and translation: The closed-loop model. In Translational control (ed. N. Sonenberg), pp. 451-480. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
19. Kahvejian, A., Roy, G., and Sonenberg, N. 2001. The mRNA closed-loop model: The function of PABP and PABP-interacting proteins in mRNA translation. Cold Spring Harb. Symp. Quant. Biol. 66: 293-300.
20. Khaleghpour, K., Kahvejian, A., De Crescenzo, G., Roy, G., Svitkin, Y.V., Imataka, H., O'Connor-McCourt, M., and Sonenberg, N. 2001a. Dual interactions of the translational repressor Paip2 with poly(A) binding protein. Mol. Cell. Biol. 21: 5200-5213.
21. Khaleghpour, K., Svitkin, Y.V., Craig, A.W., DeMaria, C.T., Deo, R.C., Burley, S.K., and Sonenberg, N. 2001b. Translational repression by a novel partner of human poly(A) binding protein, Paip2. Mol. Cell 7: 205-216.
22. Le, H., Tanguay, R.L., Balasta, M.L., Wei, C.C., Browning, K.S., Metz, A.M., Goss, D.J., and Gallie, D.R. 1997. Translation initiation factors eIF-iso4G and eIF-4B interact with the poly(A)-binding protein and increase its RNA binding activity. J. Biol. Chem. 272: 16247-16255.
23. Lee, K.A. and Sonenberg, N. 1982. Inactivation of cap-binding proteins accompanies the shut-off of host protein synthesis by poliovirus. Proc. Natl. Acad. Sci. 79: 3447-3451.
24. Lodish, H.F. and Rose, J.K. 1977. Relative importance of 7-methylguanosine in ribosome binding and translation of vesicular stomatitis virus mRNA in wheat germ and reticulocyte cell-free systems. J. Biol. Chem. 252: 1181-1188.
25. Mangus, D.A., Evans, M.C., and Jacobson, A. 2003. Poly(A)-binding proteins: Multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol. 4: 223.
26. Marcotrigiano, J., Lomakin, I.B., Sonenberg, N., Pestova, T.V., Hellen, C.U., and Burley, S.K. 2001. A conserved HEAT domain within eIF4G directs assembly of the translation initiation machinery. Mol. Cell 7: 193-203.
27. Merrick, W.C. and Sonenberg, N. 1997. Assays for eukaryotic translation factors that bind mRNA. Methods 11: 333-342.
28. Michel, Y.M., Poncet, D., Piron, M., Kean, K.M., and Borman, A.M. 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.
29. Munroe, D. and Jacobson, A. 1990. mRNA poly(A) tail, a 3′ enhancer of translational initiation. Mol. Cell. Biol. 10: 3441-3455.
30. Ostareck, D.H., Ostareck-Lederer, A., Wilm, M., Thiele, B.J., Mann, M., and Hentze, M.W. 1997. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell 89: 597-606.
31. Ostareck, D.H., Ostareck-Lederer, A., Shatsky, I.N., and Hentze, M.W. 2001. Lipoxygenase mRNA silencing in erythroid differentiation: The 3′UTR regulatory complex controls 60S ribosomal subunit joining. Cell 104: 281-290.
32. Otero, L.J., Ashe, M.P., and Sachs, A.B. 1999. The yeast poly(A)-binding protein Pab1p stimulates in vitro poly(A)-dependent and cap-dependent translation by distinct mechanisms. EMBO J. 18: 3153-3163.
33. 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.
34. Pelletier, J. and Sonenberg, N. 1985. Photochemical cross-linking of cap binding proteins to eucaryotic mRNAs: Effect of mRNA 5′ secondary structure. Mol. Cell. Biol. 5: 3222-3230.
35. Piron, M., Vende, P., Cohen, J., and Poncet, D. 1998. Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J. 17: 5811-5821.
36. Poncet, D., Aponte, C., and Cohen, J. 1993. Rotavirus protein NSP3 (NS34) is bound to the 3′ end consensus sequence of viral mRNAs in infected cells. J. Virol. 67: 3159-3165.
37. Sachs, A. 2000. Physical and functional interactions between the mRNA cap structure and the poly(A) tail. in Translational control of gene expression (ed. M.B. Mathews), pp. 447-466. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
38. Sachs, A.B. and Davis, R.W. 1989. The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation. Cell 58: 857-867.
39. Searfoss, A., Dever, T.E., and Wickner, R. 2001. Linking the 3′ poly(A) tail to the subunit joining step of translation initiation: Relations of pab1p, eukaryotic translation initiation factor 5b (Fun12p), and Ski2p-Slh1p. Mol. Cell. Biol. 21: 4900-4908.
40. Sonenberg, N. 1981. ATP/Mg++-dependent cross-linking of cap binding proteins to the 5′ end of eukaryotic mRNA. Nucleic Acids Res. 9: 1643-1656.
41. Sonenberg, N., Morgan, M.A., Merrick, W.C., and Shatkin, A.J. 1978. A polypeptide in eukaryotic initiation factors that crosslinks specifically to the 5′-terminal cap in mRNA. Proc. Natl. Acad. Sci. 75: 4843-4847.
42. Svitkin, Y.V. and Agol, V.I. 1978. Complete translation of encephalomyocarditis virus RNA and faithful cleavage of virus-specific proteins in a cell-free system from Krebs-2 cells. FEBS Lett. 87: 7-11.
43. Svitkin, Y.V. and Sonenberg, N. 2004. An efficient system for cap- and poly(A)-dependent translation in vitro. In mRNA processing and metabolism (ed. D.R. Schoenberg), pp. 155-170. Humana Press Inc., Totowa, NJ.
44. Svitkin, Y.V., Imataka, H., Khaleghpour, K., Kahvejian, A., Liebig, H.D., and Sonenberg, N. 2001a. Poly(A)-binding protein interaction with eIF4G stimulates picornavirus IRES-dependent translation. RNA 7: 1743-1752.
45. Svitkin, Y.V., Pause, A., Haghighat, A., Pyronnet, S., Witherell, G., Belsham, G.J., and Sonenberg, N. 2001b. 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.
46. Tarun, S.Z. and Sachs, A.B. 1995. A common function for mRNA 5′ and 3′ ends in translation initiation in yeast. Genes & Dev. 9: 2997-3007.
47. _. 1996. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 15: 7168-7177.
48. von Der Haar, T., Ball, P.D., and McCarthy, J.E. 2000. Stabilization of eukaryotic initiation factor 4E binding to the mRNA 5′-cap by domains of eIF4G. J. Biol. Chem. 275: 30551-30555.
49. Wakiyama, M., Imataka, H., and Sonenberg, N. 2000. Interaction of eIF4G with poly(A)-binding protein stimulates translation and is critical for Xenopus oocyte maturation. Curr. Biol. 10: 1147-1150.
50. Wei, C.C., Balasta, M.L., Ren, J., and Goss, D.J. 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.