A tale of two termini: A functional interaction between the termini of an mRNA is a prerequisite for efficient translation initiation

Gene

Volumn 216, Issue 1, 1998, Pages 1-11

  Gallie, Daniel R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Initiation factors; mRNA stability; Poly(A) binding protein; Translation

Indexed keywords

BINDING PROTEIN; INITIATION FACTOR; MESSENGER RNA; POLYADENYLIC ACID; PROTEIN SUBUNIT;

ANIMAL CELL; BINDING AFFINITY; MAMMAL CELL; MOLECULAR EVOLUTION; NONHUMAN; PLANT CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; RNA METABOLISM; RNA STRUCTURE; TRANSLATION INITIATION;

ANIMALIA; EUKARYOTA; MAMMALIA;

EID: 0032541485     PISSN: 03781119     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-1119(98)00318-7     Document Type: Article

References (79)

1. Baglioni, C., Vesco, C., Jacobs-Lorena, M., 1969. The role of ribosomal subunits in mammalian cells. Cold Spring Harbor Symp. Quant. Biol. 34, 555-566.
2. Beelman, C.A., Stevens, A., Caponigro, G., LaGrandeur, T.E., Hatfield, L., Fortner, D., Parker, R., 1996. An essential component of the decapping enzyme required for normal rates of mRNA turn-over. Nature 382, 642-646.
3. Boeck, R., Tarun, S.Z., Rieger, M., Deardorff, J.A., Muller-Auer, S., Sachs, A.B., 1996. The yeast Pan2 protein is required for poly(A)-binding protein-stimulated poly(A)-nuclease activity. J. Biol. Chem. 271, 432-438.
4. Brown, C.E., Tarun, S.Z., Boeck, R., Sachs, A.B., 1996. PAN3 encodes a subunit of the Pab1p-dependent poly(A) nuclease in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 5744-5753.
5. Caponigro, G., Parker, R., 1995. Multiple functions for the poly(A)-binding protein in mRNA decapping and deadenylation in yeast. Genes Dev. 9, 2421-2432.
6. Carrington, J.C., Freed, D.D., 1990. Cap-independent enhancement of translation by a plant potyvirus 5′ nontranslated region. J. Virol. 64, 1590-1597.
7. Christensen, A.K., Kahn, L.E., Bourne, C.M., 1987. Circular polysomes predominate on the rough endoplasmic reticulum of somatotropes and mammotropes in the rat anterior pituitary. Am. J. Anat. 178, 1-10.
8. Couttet, P., Fromont-Racine, M., Steel, D., Pictet, R., Grange, T., 1997. Messenger RNA deadenylation precedes decapping in mammalian cells. Proc. Natl. Acad. Sci. USA 94, 5628-5633.
9. Craig, A.W.B., Haghighat, A., Yu, A.T.K., Sonenberg, N., 1998. Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature 392, 520-523.
10. Crick, F.H.C., 1958. On protein synthesis. Symp. Soc. Exp. Biol. 12, 138-163.
11. Decker, C.J., Parker, R., 1993. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev. 7, 1632-1643.
12. Duncan, R., Hershey, J.W.B., 1984. Heat shock-induced translational alterations in HeLa cells. Initiation factor modifications and the inhibition of translation. J. Biol. Chem. 259, 11882-11889.
13. Duncan, R., Hershey, J.W.B., 1989. Protein synthesis and protein phosphorylation during heat stress, recovery, and adaptation. J. Cell. Biol. 109, 1467-1481.
14. Ehrenfeld, E., 1996. Initiation of translation by picornavirus RNAs. In: Mathews, M.B., Sonenberg, N., Hershey, J.W.B. (Eds.), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 549-574.
15. Francke, C., Edstrom, J.-E., McDowall, A.W., Miller Jr, O.L., 1982. Electron microscopic visualization of a discrete class of giant translation units in salivary gland cells of Chironomus tentans. EMBO J. 1, 59-62.
16. Gallie, D.R., 1991. The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 5, 2108-2116.
17. Gallie, D.R., Caldwell, C., Pitto, L., 1995a. Heat shock disrupts cap and poly(A) tail function during translation and increases mRNA stability of introduced reporter mRNA. Plant Physiol. 108, 1703-1713.
18. Gallie, D.R., Kobayashi, M., 1994. The role of the 3′-untranslated region of non-polyadenylated plant viral mRNAs in regulating translational efficiency. Gene 142, 159-165.
19. Gallie, D.R., Le, H., Caldwell, C., Tanguay, R.L., Hoang, N.X., Browning, K.S., 1997. The phosphorylation state of translation initiation factors is regulated developmentally and following heat shock in wheat. J. Biol. Chem. 272, 1046-1053.
20. Gallie, D.R., Lewis, N.J., Marzluff, W.F., 1996. The histone 3′-terminal stem-loop is necessary for translation in Chinese hamster ovary cells. Nucleic Acids Res. 24, 1954-1962.
21. Gallie, D.R., Tanguay, R., 1994. Poly(A) binds to initiation factors and increases cap-dependent translation in vitro. J. Biol. Chem. 269, 14465-14472.
22. Gallie, D.R., Tanguay, R., Leathers, V., 1995b. The tobacco etch viral 5′ leader and poly(A) tail are functionally synergistic regulators of translation. Gene 165, 233-238.
23. Gallie, D.R., Traugh, J., 1994. Serum and insulin regulate cap function in 3T3-L1 cells. J. Biol. Chem. 269, 7174-7179.
24. Gallie, D.R., Walbot, V., 1990. RNA pseudoknot domain of tobacco mosaic virus can functionally substitute for a poly(A) tail in plant and animal cells. Genes Dev. 4, 1149-1157.
25. Gradi, A., Imataka, H., Svitkin, Y.V., Rom, E., Raught, B., Morino, S., Sonenberg, N., 1998. A novel functional human eukaryotic translation initiation factor 4G. Mol. Cell. Biol. 18, 334-342.
26. Grant, C.M., Hinnebusch, A.G., 1994. Effect of sequence context at stop codons on efficiency of reinitiation in GCN4 translational control. Mol. Cell. Biol. 14, 606-618.
27. Grossi de Sa, M.-F., Standart, N., Martins de Sa, C., Akhayat, O., Huesca, M., Scherrer, K., 1988. The poly(A)-binding protein facilitates in vitro translation of poly(A)-rich mRNA. Eur. J. Biochem. 176, 521-526.
28. Haghighat, A., Sonenberg, N., 1997. eIF4G dramatically enhances the binding of eIF4E to the mRNA 5′-cap structure. J. Biol. Chem. 272, 21677-21680.
29. Hinnebusch, A., 1996. Translational control of GCN4: gene-specific regulation of phosphorylation of eIF-2. In: Hershey, J.W.B., Mathews, M.B., Sonenberg, N. (Eds.), Translational Control. Cold Spring Harbor Press, Cold Spring Harbor, NY, pp. 199-244.
30. Iizuka, N., Najita, L., Franzusoff, A., 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.
31. Imataka, H., 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.
32. Jacobson, A., Favreau, M., 1983. Possible involvement of poly(A) in protein synthesis. Nucleic Acids Res. 11, 6353-6368.
33. Jacobson, A., 1996. Poly(A) metabolism and translation: the closed-loop model. In: Hershey, J.W.B., Mathews, M.B., Sonenberg, N. (Eds.), Translational Control. Cold Spring Harbor Press, Cold Spring Harbor, NY, pp. 451-480.
34. Joshi, B., Yan, R., Rhoads, R.E., 1994. In vitro synthesis of human protein synthesis initiation factor 4γ and its localization on 43 and 48 S initiation complexes. J. Biol. Chem. 269, 2048-2055.
35. Kessler, S.H., Sachs, A.B., 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.
36. Kiseleva, E.V., 1989. Secretory protein synthesis in Chironomus salivary gland cells is not coupled with protein translocation across endoplasmic reticulum membranes. FEBS Lett. 257, 251-253.
37. Kozak, M., 1986. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44, 283-292.
38. Lamphear, B.J., Kirchweger, R., Skern, T., Rhoads, R.E., 1995. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases - implications for cap-dependent and cap-independent translational initiation. J. Biol. Chem. 270, 21975-21983.
39. Lamphear, B.J., Panniers, R., 1990. Cap binding protein complex that restores protein synthesis in heat-shocked Ehrlich cell lysates contains highly phosphorylated eIF-4E. J. Biol. Chem. 265, 5333-5336.
40. Lamphear, B.J., Panniers, R., 1991. Heat shock impairs the interaction of cap-binding protein complex with 5′ mRNA cap. J. Biol. Chem. 266, 2789-2794.
41. Le, H., Tanguay, R.L., Balasta, M.L., Wei, C.-C., Browning, K.S., Metz, A.M., Goss, D.J., Gallie, D.R., 1997. The translation initiation factors eIFiso4G and eIF-4B interact with the poly(A)-binding protein to increase its RNA binding affinity. J. Biol. Chem. 272, 16247-16255.
42. Leathers, V., Tanguay, R., Kobayashi, M., Gallie, D.R., 1993. A phylogenetically conserved sequence within viral 3′ untranslated RNA pseudoknots regulates translation. Mol. Cell. Biol. 13, 5331-5347.
43. Lin, T.-A., Kong, X., Haystead, T.A.J., Pause, A., Belsham, G., Sonenberg, N., Lawrence, J.C., 1994. PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 266, 653-656.
44. Lodish, H.F., Nathan, D.G., 1972. Regulation of hemoglobin synthesis. Preferential inhibition of and globin synthesis. J. Biol. Chem. 247, 7822-7829.
45. Lowell, J.E., Rudner, D.Z., Sachs, A.B., 1992. 3′-UTR-dependent deadenylation by the yeast poly(A) nuclease. Genes Dev. 6, 2088-2099.
46. Manzella, J.M., Rychlik, W., Rhoads, R.E., Hershey, J.W.B., Blackshear, P.J., 1991. Insulin induction of ornithine decarboxylase. J. Biol. Chem. 266, 2382-2389.
47. Marzluff, W.F., 1992. Histone 3′ ends: essential and regulatory functions. Gene Exp. 2, 93-97.
48. Merrick, W.C., Hershey, J.W.B., 1996. The pathway and mechanism of eukaryotic protein synthesis. In: Hershey, J.W.B., Mathews, M.B., Sonenberg, N. (Eds.), Translational Control. Cold Spring Harbor Press, Cold Spring Harbor, NY, pp. 31-69.
49. Metz, A.M., Browning, K.S., 1996. Mutational analysis of the functional domains of the large subunit of the isozyme form of wheat initiation factor eIF4F. J. Biol. Chem. 271, 31033-31036.
50. Minich, W., Balasta, M.L., Goss, D.J., Rhoads, R.E., 1994. Chromatographic resolution of in vivo phosphorylated and nonphosphorylated eukaryotic translation initiation factor eIF-4E: increased cap affinity of the phosphorylated form. Proc. Natl. Acad. Sci. USA 91, 7668-7672.
51. Morley, S.J., Traugh, J.A., 1990. Differential stimulation of phosphorylation of initiation factors eIF-4F, eIF-4B, eIF-3, and ribosomal protein S6 by insulin and phorbol esters. J. Biol. Chem. 265, 10611-10616.
52. Muhlrad, D., Decker, C.J., Parker, R., 1995. Turnover mechanisms of the stable yeast PGK1 mRNA. Mol. Cell. Biol. 15, 2145-2156.
53. Muhlrad, D., Decker, C.J., Parker, R., 1994. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′→3′ digestion of the transcript. Genes Dev. 8, 855-866.
54. Muhlrad, D., Parker, R., 1992. Mutations affecting stability and deadenylation of the yeast MFA2 transcript. Genes Dev. 6, 2100-2111.
55. Munroe, D., Jacobson, A., 1990a. Tales of poly(A): a review. Gene 91, 151-158.
56. Munroe, D., Jacobson, A., 1990b. mRNA poly(A) tail, a 3′ enhancer of translational initiation. Mol. Cell. Biol. 10, 3441-3455.
57. Ohlmann, T., Rau, M., Pain, V.M., Morley, S.J., 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, 1371-1382.
58. Pain, V.M., 1996. Initiation of protein synthesis in eukaryotic cells. Eur. J. Biochem. 236, 747-771.
59. Palade, G., 1955. A small particulate component of the cytoplasm. J. Biophys. Biochem. Cytol. 1, 59-67.
60. Palade, G., 1975. Intracellular aspects of the process of protein synthesis. Science 189, 347-358.
61. Panniers, R., Stewart, E.B., Merrick, W.C., Henshaw, E.C., 1985. Mechanism of inhibition of polypeptide chain initiation in heat-shocked Ehrlich cells involves reduction of eukaryotic initiation factor 4F activity. J. Biol. Chem. 260, 9648-9653.
62. Pause, A., Belsham, G., Gingras, A.-C., Donze, O., Lin, T.-A., Lawrence, J.C., Sonenberg, N., 1994. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371, 762-777.
63. Philipps, G.R., 1965. Haemoglobin synthesis and polysomes in intact reticulocytes. Nature 205, 567-570.
64. Preiss, T., Hentze, M.W., 1998. Dual function of the messenger RNA cap structure in poly(A)-tail-promoted translation in yeast. Nature 392, 516-520.
65. Proweller, A., Butler, J.S., 1996. Ribosomal association of poly(A)-binding protein in poly(A)-deficient Saccharomyces cerevisiae. J. Biol. Chem. 271, 10859-10865.
66. Ray, B.K., Lawson, T.G., Kramer, J.C., Cladaras, M.H., Grifco, J.A., Abramson, R.D., Merrick, W.C., Thach, R.E., 1985. ATP-dependent unwinding of messenger RNA structure by eukaryotic initiation factors. J. Biol. Chem. 260, 7651-7658.
67. Roberts, R.B., 1958. In: Roberts, R.B. (Ed.), Microsomal Particles and Protein Synthesis. Pergamon, New York, pp. vii-viii.
68. Sachs, A.B., 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.
69. Sachs, A.B., Davis, R.W., 1990. Translation initiation and ribosomal biogenesis: involvement of a putative rRNA helicase and RPL46. Science 247, 1077-1079.
70. Shatkin, A.J., Darzynkiewicz, E., Furuichi, Y., Kroath, H., Morgan, M.A., Tahara, S.M., Yamakawa, M., 1982. 5′-Terminal caps, cap-binding proteins and eukaryotic mRNA function. Biochem. Soc. Symp. 47, 129-143.
71. Tanguay, R.L., Gallie, D.R., 1996a. Translational efficiency is regulated by the length of the 3′ untranslated region. Mol. Cell. Biol. 16, 146-156.
72. Tanguay, R.L., Gallie, D.R., 1996b. The effect of the length of the 3′-untranslated region on expression in plants. FEBS Lett. 394, 285-288.
73. Tarun, S.Z., Sachs, A.B., 1995. A common function for mRNA 5′ and 3′ ends in translation initiation in yeast. Genes Dev. 9, 2997-3007.
74. Tarun, S.Z., Sachs, A.B., 1996. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 15, 7168-7177.
75. Tarun, S.Z., Wells, S.E., Deardorff, J.A., Sachs, A.B., 1997. Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc. Natl. Acad. Sci. USA 94, 9046-9051.
76. van Belkum, A., Abrahams, J.P., Pleij, C.W.A., Bosch, L., 1985. Five pseudoknots are present at the 204 nucleotides long 3′ noncoding region of tobacco mosaic virus RNA. Nucleic Acids Res. 13, 7673-7686.
77. Warner, J.R., Knopf, P.M., Rich, A., 1963. A multiple ribosomal structure in protein synthesis. Proc. Natl. Acad. Sci. USA 49, 122-129.
78. Wei, C.-C., Balasta, M.L., Ren, J., 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.
79. Yang, H., Duckett, C.S., Lindsten, T., 1995. iPABP, an inducible poly(A)-binding protein detected in activated human T cells. Mol. Cell. Biol. 15, 6770-6776.