eIF4E promotes nuclear export of cyclin D1 mRNAs via an element in the 3′UTR

Journal of Cell Biology

Volumn 169, Issue 2, 2005, Pages 245-256

  Culjkovic, Biljana ^a,b   Topisirovic, Ivan ^a,b   Skrabanek, Lucy ^c   Ruiz Gutierrez, Melisa ^a,b   Borden, Katherine L B ^a,b  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; INITIATION FACTOR 4E; MESSENGER RNA; RIBONUCLEOPROTEIN;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL GROWTH; CELL MEMBRANE TRANSPORT; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOPLASM; EMBRYO; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSLATION INITIATION;

3' UNTRANSLATED REGIONS; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CELL PROLIFERATION; CYCLIN D1; CYTOPLASM; EUKARYOTIC INITIATION FACTOR-4E; HUMANS; MICE; NIH 3T3 CELLS; PROTEIN BINDING; RIBONUCLEOPROTEINS; TRANSFECTION;

ANIMALIA; EUKARYOTA;

EID: 18544363908     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200501019     Document Type: Article

References (34)

1. Boisvert, F.M., M.J. Hendzel, and D.P. Bazett-Jones. 2000. Promyelocytic leukemia (PML) nuclear bodies are protein structures that do not accumulate RNA. J. Cell Biol. 148:283-292.
2. Borden, K.L.B., M.N. Boddy, J. Lally, N.J. O'Reilly, S. Martin, K. Howe, E. Solomon, and P.S. Freemont. 1995. The solution structure of the RING finger domain from the acute promyelocytic leukaemia proto-oncoprotein PML. EMBO J. 14:1532-1541.
3. Cohen, N., M. Sharma, A. Kentsis, J.M. Perez, S. Strudwick, and K.L. Borden. 2001. PML RING suppresses oncogenic transformation by reducing the affinity of eIF4E for mRNA. EMBO J. 20:4547-4559.
4. Dostie, J., M. Ferraiuolo, A. Pause, S.A. Adam, and N. Sonenberg. 2000. A novel shuttling protein, 4E-T, mediates the nuclear import of the mRNA 5′ cap-binding protein, eIF4E. EMBO J. 19:3142-3156.
5. Gingras, A.C., B. Raught, and N. Sonenberg. 1999. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68:913-963.
6. Iborra, F.J., D.A. Jackson, and P.R. Cook. 2001. Coupled transcription and translation within nuclei of mammalian cells. Science. 293:1139-1142.
7. Ishigaki, Y., X. Li, G. Serin, and L.E. Maquat. 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.
8. Izaurralde, E., J. Lewis, C. Gamberi, A. Jarmolowski, C. McGuigan, and I.W. Mattaj. 1995. A cap-binding protein complex mediating U snRNA export. Nature. 376:709-712.
9. Kentsis, A., E.C. Dwyer, J.M. Perez, M. Sharma, A. Chen, Z.Q. Pan, and K.L. Borden. 2001. The RING domains of the promyelocytic leukemia protein PML and the arenaviral protein z repress translation by directly inhibiting translation initiation factor eIF4E. J. Mol. Biol. 312:609-623.
10. Kentsis, A., I. Topisirovic, B. Culjkovic, L. Shao, and K.L. Borden. 2004. Ribavirin suppresses eIF4E-mediated oncogenic transformation by physical mimicry of the 7-methyl guanosine mRNA cap. Proc. Natl. Acad. Sci. USA. 101:18105-18110.
11. Lai, H.K., and K.L. Borden. 2000. The promyelocytic leukemia (PML) protein suppresses cyclin D1 protein production by altering the nuclear cytoplasmic distribution of cyclin D1 mRNA. Oncogene. 19:1623-1634.
12. Lang, V., N.I. Zanchin, H. Lunsdorf, M. Tuite, and J.E. McCarthy. 1994. Initiation factor eIF-4E of Saccharomyces cerevisiae. Distribution within the cell, binding to mRNA, and consequences of its overproduction. J. Biol. Chem. 269:6117-6123.
13. Lazaris-Karatzas, A., K.S. Montine, and N. Sonenberg. 1990. Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5′ cap. Nature. 345:544-547.
14. Lazaris-Karatzas, A., and N. Sonenberg. 1992. The mRNA 5′ cap-binding protein, eIF-4E, cooperates with v-myc or E1A in the transformation of primary rodent fibroblasts. Mol. Cell. Biol. 12:1234-1238.
15. Lejbkowicz, F., C. Goyer, A. Darveau, S. Neron, R. Lemieux, and N. Sonenberg. 1992. A fraction of the mRNA 5′ cap-binding protein, eukaryotic initiation factor 4E, localizes to the nucleus. Proc. Natl. Acad. Sci. USA. 89:9612-9616.
16. Lejeune, F., Y. Ishigaki, X. Li, and L.E. Maquat. 2002. The exon junction complex is detected on CBP80-bound but not eIF4E-bound mRNA in mammalian cells: dynamics of mRNP remodeling. EMBO J. 21:3536-3545.
17. Marcotrigiano, J., A.C. Gingras, N. Sonenberg, and S.K. Burley. 1997. Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell. 89:951-961.
18. McKendrick, L., E. Thompson, J. Ferreira, S.J. Morley, and J.D. Lewis. 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.
19. Morley, S.J., and V.M. Pain. 1995. Hormone-induced meiotic maturation in Xenopus oocytes occurs independently of p70s6k activation and is associated with enhanced initiation factor (eIF)-4F phosphorylation and complex formation. J. Cell Sci. 108:1751-1760.
20. Motokura, T., and A. Arnold. 1993. PRAD1/cyclin D1 proto-oncogene: genomic organization, 5′ DNA sequence, and sequence of a tumor-specific rearrangement breakpoint. Genes Chromosomes Cancer. 7:89-95.
21. Nathan, C.A., P. Carter, L. Liu, B.D. Li, F. Abreo, A. Tudor, S.O. Zimmer, and A. De Benedetti. 1997. Elevated expression of eIF4E and FGF-2 isoforms during vascularization of breast carcinomas. Oncogene. 15:1087-1094.
22. Perez-Roger, I., S.H. Kim, B. Griffiths, A. Sewing, and H. Land. 1999. Cyclins D1 and D2 mediate myc-induced proliferation via sequestration of p27(Kip1) and P21(Cip1). EMBO J. 18:5310-5320.
23. Rousseau, D., R. Kaspar, I. Rosenwald, L. Gehrke, and N. Sonenberg. 1996. Translation initiation of ornithine decarboxylase and nucleocytoplasmic transport of cyclin D1 mRNA are increased in cells overexpressing eukaryotic initiation factor 4E. Proc. Natl. Acad. Sci. USA. 93:1065-1070.
24. Sonenberg, N., and A.C. Gingras. 1998. The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Curr. Opin. Cell Biol. 10:268-275.
25. Spector, D.L., R.D. Goldman, and L.A. Leinwand. 1998. Cells: A Laboratory Manual. Cold Spring Harbor, Cold Spring Harbor, NY. 116.8-116.16.
26. Strudwick, S., and K.L. Borden. 2002. The emerging roles of translation factor eIF4E in the nucleus. Differentiation. 70:10-22.
27. Stuurman, N., A. de Graaf, A. Floore, A. Josso, B. Humbel, L. de Jong, and R. van Driel. 1992. A monoclonal antibody recognizing nuclear matrix-associated nuclear bodies. J. Cell Sci. 101:773-784.
28. Thompson, J.D., D.G. Higgins, and T.J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
29. Topisirovic, I., A.D. Capili, and K.L. Borden. 2002. Gamma Interferon and cadmium treatments modulate eukaryotic initiation factor 4E-dependent mRNA transport of cyclin D1 in a PML-dependent manner. Mol. Cell. Biol. 22:6183-6198.
30. Topisirovic, I., B. Culjkovic, N. Cohen, J.M. Perez, L. Skrabanek, and K.L. Borden. 2003a. The proline-rich homeodomain protein, PRH, is a tissue-specific inhibitor of eIF4E-dependent cyclin D1 mRNA transport and growth. EMBO J. 22:689-703.
31. Topisirovic, I., M.L. Guzman, M.J. McConnell, J.D. Licht, B. Culjkovic, S.J. Neering, C.T. Jordan, and K.L. Borden. 2003b. Aberrant eukaryotic translation initiation factor 4E-dependent mRNA transport impedes hematopoietic differentiation and contributes to leukemogenesis. Mol. Cell. Biol. 23:8992-9002.
32. Topisirovic, I., M. Ruiz-Gutierrez, and K.L.B. Borden. 2004. Phosphorylation of the eukaryotic translation initiation factor eIF4E contributes to its transformation and mRNA transport activities. Cancer Res. 64:8639-8642.
33. Trifillis, P., N. Day, and M. Kiledjian. 1999. Finding the right RNA: identification of cellular mRNA substrates for RNA-binding proteins. RNA. 5:1071-1082.
34. Visa, N., E. Izaurralde, J. Ferreira, B. Daneholt, and J.W. Mattaj. 1996. A nuclear cap-binding complex binds balbiani ring pre-mRNA cotranscriptionally and accompanies the ribonucleoprotein particle during nuclear export. J. Cell Biol. 133:5-14.