Selective recruitment of proteins to 5′ cap complexes during the growth cycle in Arabidopsis

Plant Journal

Volumn 59, Issue 3, 2009, Pages 400-412

  Bush, Maxwell S ^a   Hutchins, Andrew P ^a,d   Jones, Alexandra M E ^b   Naldrett, Mike J ^a   Jarmolowski, Artur ^c   Lloyd, Clive W ^a   Doonan, John H ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b SAINSBURY LABORATORY   (United Kingdom)

^c ADAM MICKIEWICZ UNIVERSITY   (Poland)

^d GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

Arabidopsis; Cap complex; Growth cycle; Proteomics; Translation; Translation initiation factor

Indexed keywords

ARABIDOPSIS PROTEIN; CAPPED RNA; CBP80 PROTEIN, ARABIDOPSIS; INITIATION FACTOR 4E; MESSENGER RNA; PLANT RNA; RNA BINDING PROTEIN; RNA HELICASE;

ARABIDOPSIS; ARTICLE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROTEIN SYNTHESIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; EUKARYOTIC INITIATION FACTOR-4E; PROTEIN BIOSYNTHESIS; RNA CAPS; RNA HELICASES; RNA, MESSENGER; RNA, PLANT; RNA-BINDING PROTEINS;

ANIMALIA; ARABIDOPSIS;

EID: 67651207956     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.03882.x     Document Type: Article

References (61)

1. Belostotsky, D.A. Rose, A.B. (2005) Plant gene expression in the age of systems biology: integrating transcriptional and post-transcriptional events. Trends Plant Sci. 10, 347 353.
2. Bi, X., Ren, J. Goss, D.J. (2000) Wheat germ translation initiation factor eIF4B affects eIF4A and eIFiso4F helicase activity by increasing the ATP binding affinity of eIF4A. Biochemistry, 39, 5758 5765.
3. Browning, K.S. (1996) The plant translational apparatus. Plant Mol. Biol. 32, 107 144.
4. Browning, K.S. (2004) Plant translation initiation factors: it is not easy to be green. Biochem. Soc. Trans. 32, 589 591.
5. Carberry, S.E. Goss, D.J. (1991) Wheat germ initiation factors 4F and (iso)4F interact differently with oligoribonucleotide analogues of rabbit α-globin mRNA. Biochemistry, 30, 4542 4545.
6. Carberry, S.E., Darzynkiewicz, E. Goss, D.J. (1991) A comparison of the binding of methylated cap analogues to wheat germ protein synthesis initiation factors 4F and (iso)4F. Biochemistry, 30, 1624 1627.
7. Chiu, S.Y., Lejeune, F., Ranganathan, A.C. Maquat, L.E. (2004) The pioneer translation initiation complex is functionally distinct from but structurally overlaps with the steady-state translation initiation complex. Genes Dev. 18, 745 754.
8. Cléry, A., Blatter, M. Allain, F.H.-T. (2008) RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 18, 290 298.
9. Delannoy, E., Stanley, W.A., Bond, C.S. Small, I.D. (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem. Soc. Trans. 35, 1643 1647.
10. Ding, Y.H., Liu, N.Y., Tang, Z.S., Liu, J. Yang, W.C. (2006) Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell, 18, 815 830.
11. Dinkova, T.D., Aguilar, R. Sanchez de Jimenez, E. (2000) Expression of maize eukaryotic initiation factor (eIF) iso4E is regulated at the translational level. Biochem. J. 351, 825 831.
12. Dostie, J., Lejbkowicz, F. Sonenberg, N. (2000) Nuclear eukaryotic initiation factor 4E (eIF4E) colocalizes with splicing factors in speckles. J. Cell Biol. 148, 239 247.
13. Fan, H. Penman, S. (1970) Regulation of protein synthesis in mammalian cells. II. Inhibition of protein synthesis at the level of initiation during mitosis. J. Mol. Biol. 50, 655 670.
14. Fedoroff, N.V. (2002) RNA-binding proteins in plants: the tip of an iceberg? Curr. Opin. Plant Biol. 5, 452 459.
15. Fortes, P., Inada, T., Preiss, T., Hentze, M.W., Mattaj, I.W. Sachs, A.B. (2000) The yeast nuclear cap binding complex can interact with translation factor eIF4G and mediate translation initiation. Mol. Cell, 6, 191 196.
16. Frydman, J. (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu. Rev. Biochem. 70, 603 647.
17. Fusaro, A.F., Bocca, S.N., Ramos, R.L. et al. (2007) AtGRP2, a cold-induced nucleo-cytoplasmic RNAbinding protein, has a role in flower and seed development. Planta, 225, 1339 1351.
18. Gallie, D.R. (2001) Cap-independent translation conferred by the 5′ leader of tobacco etch virus is eukaryotic initiation factor 4G dependent. J. Virol. 75, 12141 12152.
19. Gallie, D.R. Browning, K.S. (2001) eIF4G functionally differs from eIFiso4G in promoting internal initiation, cap-independent translation, and translation of structured mRNAs. J. Biol. Chem. 276, 36951 36960.
20. Gingras, A.C., Raught, B. Sonenberg, N. (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68, 913 963.
21. Gray, N.K. Wickens, M. (1998) Control of translation initiation in animals. Annu. Rev. Cell Dev. Biol. 14, 399 458.
22. Healy, J.M., Menges, M., Doonan, J.H. Murray, J.A. (2001) The Arabidopsis D-type cyclins CycD2 and CycD3 both interact in vivo with the PSTAIRE cyclin-dependent kinase Cdc2a but are differentially controlled. J. Biol. Chem. 276, 7041 7047.
23. Herr, A.J., Molnar, A., Jones, A. Baulcombe, D.C. (2006) Defective RNA processing enhances RNA silencing and influences flowering of Arabidopsis. Proc. Natl Acad Sci. USA, 103, 14997 15001.
24. Huang, Y.-S., Kan, M.-C., Lin, C.-L. Richter, J.D. (2006) CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA. EMBO J. 25, 4865 4876.
25. Hugouvieux, V., Kwak, J.M. Schroeder, J.I. (2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell, 106, 477 487.
26. Hutchins, A.P., Roberts, G.R., Lloyd, C.W. Doonan, J.H. (2004) In vivo interaction between CDKA and eIF4A: a possible mechanism linking translation and cell proliferation. FEBS Lett. 556, 91 94.
27. Ishigaki, Y., Li, X., Serin, G. Maquat, L.E. (2001) Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell, 106, 607 617.
28. Izaurralde, E. Mattaj, I.W. (1995) RNA export. Cell, 81, 153 159.
29. Kalifa, Y., Huang, T., Rosen, L.N., Chatterjee, S. Gavis, E.R. (2006) Glorund, a Drosophila hnRNP F/H homolog, is an ovarian repressor of nanos translation. Dev. Cell, 10, 291 301.
30. Kawaguchi, R. Bailey-Serres, J. (2002) Regulation of translational initiation in plants. Curr. Opin. Plant Biol. 5, 460 465.
31. Khan, M.A., Miyoshi, H., Gallie, D.R. Goss, D.J. (2008) Potyvirus genomelinked protein, VPg, directly affects wheat germ in vitro translation: interactions with translation initiation factors eIF4F and eIFiso4F. J. Biol. Chem. 283, 1340 1349.
32. Kierzkowski, D., Kmieciak, M., Piontek, P., Wojtaszek, P., Szweykowska-Kulinska, Z. Jarmolowski, A. (2009) Arabidopsis CBP20 targets the cap-binding complex to the nucleus and is stabilized by CBP80. Plant J., in press.
33. Kmieciak, M., Simpson, C.G., Lewandowska, D., Brown, J.W. Jarmolowski, A. (2002) Cloning and characterization of two subunits of Arabidopsis thaliana nuclear cap-binding complex. Gene, 283, 171 183.
34. Koromilas, A.E., Lazaris-Karatzas, A. Sonenberg, N. (1992) mRNAs containing extensive secondary structure in their 5′ non-coding region translate efficiently in cells overexpressing initiation factor eIF-4E. EMBO J. 11, 4153 4158.
35. Lejeune, F., Ranganathan, A.C. Maquat, L.E. (2004) eIF4G is required for the pioneer round of translation in mammalian cells. Nature Struct. Mol. Biol. 11, 992 1000.
36. Lu, J.-Y., Bergman, N., Sadri, N. Schneider, R.J. (2006) Assembly of AUF1 with eIF4G-poly(A) binding protein complex suggests a translation function in AU-rich mRNA decay. RNA, 12, 883 893.
37. Mazza, C., Ohno, M., Segref, A., Mattaj, I.W. Cusack, S. (2001a) Crystal structure of the human nuclear cap binding complex. Mol. Cell, 8, 383 396.
38. McKendrick, L., Thompson, E., Ferreira, J., Morley, S.J. Lewis, J.D. (2001) Interaction of eukaryotic translation initiation factor 4G with the nuclear cap-binding complex provides a link between nuclear and cytoplasmic functions of the m(7) guanosine cap. Mol. Cell. Biol. 21, 3632 3641.
39. Menges, M., Hennig, L., Gruissem, W. Murray, J.A. (2003) Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol. Biol. 53, 423 442.
40. 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.
41. Miyoshi, H., Okade, H., Muto, S., Suehiro, N., Nakashima, H., Tomoo, K. Natsuaki, T. (2008) Turnip mosaic virus VPg interacts with Arabidopsis thaliana eIF(iso)4E and inhibits in vitro translation. Biochimie, 90, 1427 1434.
42. Nishizawa, K., Freund, C., Li, J., Wagner, G. Reinherz, E.L. (1998) Identification of a proline-binding motif regulating CD2-triggered T lymphocyte activation. Proc. Natl Acad. Sci. USA, 95, 14897 14902.
43. Papp, I., Mur, L.A., Dalmadi, A., Dulai, S. Koncz, C. (2004) A mutation in the Cap binding protein 20 gene confers drought tolerance to Arabidopsis. Plant Mol. Biol. 55, 679 686.
44. Pause, A. Sonenberg, N. (1992) Mutational analysis of a DEAD box RNA helicase: the mammalian translation initiation factor eIF-4A. EMBO J. 11, 2643 2654.
45. Pause, A., Methot, N., Svitkin, Y., Merrick, W.C. 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.
46. Perkins, D.N., Pappin, D.J., Creasy, D.M. Cottrell, J.S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis, 20, 3551 3567.
47. Pestova, T.V., Kolupaeva, V.G., Lomakin, I.B., Pilipenko, E.V., Shatsky, I.N., Agol, V.I. Hellen, C.U. (2001) Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl Acad. Sci. USA, 98, 7029 7036.
48. Ponting, C.P. (2000) Novel eIF4G domain homologues linking mRNA translation with nonsense-mediated mRNA decay. Trends Biochem. Sci. 25, 423 426.
49. Pyronnet, S., Dostie, J. Sonenberg, N. (2001) Suppression of cap-dependent translation in mitosis. Genes Dev. 15, 2083 2093.
50. Ray, S., Yumak, H., Domashevskiy, A., Khan, M.A., Gallie, D.R. Goss, D.J. (2006) Tobacco etch virus mRNA preferentially binds wheat germ eukaryotic initiation factor (eIF) 4G rather than eIFiso4G. J. Biol. Chem. 281, 35826 35834.
51. Richard, C., Granier, C., Inze, D. De Veylder, L. (2001) Analysis of cell division parameters and cell cycle gene expression during the cultivation of Arabidopsis thaliana cell suspensions. J. Exp. Bot. 52, 1625 1633.
52. Rodriguez, C.M., Freire, M.A., Camilleri, C. Robaglia, C. (1998) The Arabidopsis thaliana cDNAs coding for eIF4E and eIF(iso)4E are not functionally equivalent for yeast complementation and are differentially expressed during plant development. Plant J. 13, 465 473.
53. Rong, L., Livingstone, M., Sukarieh, R. et al. (2008) Control of eIF4E cellular localization by eIF4E-binding proteins, 4E-BPs. RNA, 14, 1318 1327.
54. Ruud, K.A., Kuhlow, C., Goss, D.J. Browning, K.S. (1998) Identification and characterization of a novel cap-binding protein from Arabidopsis thaliana. J. Biol. Chem. 273, 10325 10330.
55. Saha, D., Prasad, A.M. Srinivasan, R. (2007) Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol. Biochem. 45, 521 534.
56. Scheper, G.C., van Kollenburg, B., Hu, J., Luo, Y., Goss, D.J. Proud, C.G. (2002) Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affinity for capped mRNA. J. Biol. Chem. 277, 3303 3309.
57. Schoning, J.C., Streitner, C., Meyer, I.M., Gao, Y. Staiger, D. (2008) Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis. Nucleic Acids Res. 36, 6977 6987.
58. Simmons, H.M., Ruis, B.L., Kapoor, M., Hudacek, A.W. Conklin, K.F. (2005) Identification of NOM1, a nucleolar, eIF4A binding protein encoded within the chromosome 7q36 breakpoint region targeted in cases of pediatric acute myeloid leukemia. Gene, 347, 137 145.
59. Sonenberg, N. Gingras, A.C. (1998) The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Curr. Opin. Cell Biol. 10, 268 275.
60. Van Leene, J., Stals, H., Eeckhout, D. et al. (2007) A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol. Cell Proteomics, 6, 1226 1238.
61. Varani, G. (1997) A cap for all occasions. Structure, 5, 855 858.