A co-repressor assembly nucleated by Sex-lethal in the 3′UTR mediates translational control of Drosophila msl-2 mRNA

EMBO Journal

Volumn 22, Issue 20, 2003, Pages 5571-5581

  Grskovic, Marica ^a   Hentze, Matthias W ^a   Gebauer, Fátima ^b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

Author keywords

Dosage compensation; In vitro translation; Post transcriptional control; RNA protein interactions; RNPs

Indexed keywords

HEPTAPEPTIDE; MESSENGER RNA; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CROSS LINKING; DROSOPHILA; GENE EXPRESSION REGULATION; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA BINDING; SEX DETERMINATION; TRANSLATION INITIATION; TRANSLATION REGULATION; X CHROMOSOME;

3' UNTRANSLATED REGIONS; ANIMALS; CLONING, MOLECULAR; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; ESCHERICHIA COLI; INSECT HORMONES; MALE; NUCLEAR PROTEINS; PROTEIN BIOSYNTHESIS; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0142105380     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg539     Document Type: Article

References (44)

1. Akhtar, A. (2003) Dosage compensation: an intertwined world of RNA and chromatin remodelling. Curr. Opin. Genet. Dev., 13, 161-169.
2. Bashaw, G.J. and Baker, B.S. (1995) The msl-2 dosage compensation gene of Drosophila encodes a putative DNA-binding protein whose expression is sex specifically regulated by Sex-lethal. Development, 121, 3245-3258.
3. Bashaw, G.J. and Baker, B.S. (1997) The regulation of the Drosophila msl-2 gene reveals a function for Sex-lethal in translational control. Cell, 89, 789-798.
4. Bell, L.R., Horabin, J.I. Schedl, P. and Cline, T.W. (1991) Positive autoregulation of sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell, 65, 229-239.
5. Crowder, S.M., Kanaar, R., Rio, D.C. and Alber, T. (1999) Absence of interdomain contacts in the crystal structure of the RNA recognition motifs of Sex-lethal. Proc. Natl Acad. Sci. USA, 96, 4892-4897.
6. De Gregorio, E., Baron, J., Preiss, T. and Hentze, M.W. (2001) Tethered-function analysis reveals that elF4E can recruit ribosomes independent of its binding to the cap structure. RNA, 7, 106-113.
7. Deshpande, G., Samuels, M.E. and Schedl, P.D. (1996) Sex-lethal interacts with splicing factors in vitro and in vivo. Mol. Cell Biol., 16, 5036-5047
8. Deshpande, G., Calhoun, G., Yanowitz, J.L. and Schedl, P.D. (1999) Novel functions of nanos in downregulating mitosis and transcription during the development of the Drosophila germline. Cell, 99, 271-281.
9. Dong, Z. and Bell, L.R. (1999) SIN, a novel Drosophila protein that associates with the RNA binding protein sex-lethal. Gene, 237, 421-428.
10. Gebauer, F., Merendino, L., Hentze, M.W. and Valcárcel, J. (1998) The Drosophila splicing regulator sex-lethal directly inhibits translation of male-specific-lethal 2 mRNA. RNA, 4, 142-150.
11. Gebauer, F., Corona, D.F., Preiss, T., Becker, P.B. and Hentze, M.W. (1999) Translational control of dosage compensation in Drosophila by Sex-lethal: cooperative silencing via the 5′ and 3′ UTRs of msl-2 mRNA is independent of the poly(A) tail. EMBO J., 18, 6146-6154.
12. Gebauer, F., Grskovic, M. and Hentze, M.W. (2003) Drosophila Sex-Lethal Inhibits the stable association of the 40S ribosomal subunit with msl-2 mRNA. Mol. Cell, 11, 1397-1404.
13. Gehring, N.H., Neu-Yilik, G., Schell, T., Hentze, M.W. and Kulozik, A.E. (2003) Y14 and hUpf3b form an NMD-activating complex. Mol. Cell, 11, 939-949.
14. Gray, N.K. and Hentze, M.W. (1994) Regulation of protein synthesis by mRNA structure. Mol. Biol. Rep., 19, 195-200.
15. 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.
16. Handa, N., Nureki, O., Kurimoto, K., Kim, I., Sakamoto, H., Shimura, Y., Muto, Y. and Yokoyama, S. (1999) Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature, 398, 579-585.
17. Kanaar, R., Lee, A.L., Rudner, D.Z., Wemmer, D.E. and Rio, D.C. (1995) Interaction of the sex-lethal RNA binding domains with RNA. EMBO J., 14, 4530-4539.
18. Kelley, R.L., Wang, J., Bell, L. and Kuroda, M.I. (1997) Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature, 387, 195-199.
19. Kim, I. et al. (2000) Interactions of a didomain fragment of the Drosophila sex-lethal protein with single-stranded uridine-rich oligoribonucleotides derived from the transformer and Sex-lethal messenger RNA precursors: NMR with residue-selective [5-2H]uridine substitutions. J. Biomol. NMR, 17, 153-165.
20. Lallena, M.J., Chalmers, K.J., Llamazares, S., Lamond, A.I. and Valcárcel, J. (2002) Splicing regulation at the second catalytic step by Sex-lethal involves 3′ splice site recognition by SPF45. Cell, 109, 285-296.
21. Lee, A.L., Volkman, B.F., Robertson, S.A., Rudner, D.Z., Barbash, D.A., Cline, T.W., Kanaar, R., Rio, D.C. and Wemmer, D.E. (1997) Chemical shift mapping of the RNA-binding interface of the multiple-RBD protein sex-lethal. Biochemistry, 36, 14306-14317.
22. Lykke-Andersen, J., Shu, M.D. and Steitz, J.A. (2000) Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell, 103, 1121-1131.
23. Meise, M., Hilfiker-Kleiner, D., Dubendorfer, A., Brunner, C., Nothiger, R. and Bopp, D. (1998) Sex-lethal, the master sex-determining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development, 125, 1487-1494.
24. Muckenthaler, M., Gray, N.K. and Hentze, M.W. (1998) IRP-1 binding to ferritin mRNA prevents the recruitment of the small ribosomal subunit by the cap-binding complex elF4F. Mol. Cell, 2, 383-388.
25. Parks, T.D., Leuther, K.K., Howard, E.D., Johnston, S.A. and Dougherty, W.G. (1994) Release of proteins and peptides from fusion proteins using a recombinant plant virus proteinase. Anal. Biochem., 216, 413-417.
26. Sakashita, E. and Sakamoto, H. (1994) Characterization of RNA binding specificity of the Drosophila sex-lethal protein by in vitro ligand selection. Nucleic Acids Res., 22, 4082-4086.
27. Sakashita, E. and Sakamoto, H. (1996) Protein-RNA and protein-protein interactions of the Drosophila sex-lethal mediated by its RNA-binding domains. J. Biochem., 120, 1028-1033.
28. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbour, NY.
29. Samuels, M., Deshpande, G. and Schedl, P. (1998) Activities of the Sex-lethal protein in RNA binding and protein:protein interactions. Nucleic Acids Res., 26, 2625-2637.
30. Schutt, C. and Nothiger, R. (2000) Structure, function and evolution of sex-determining systems in Dipteran insects. Development, 127, 667-677.
31. Singh, R., Valcárcel, J. and Green, M.R. (1995) Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science, 268, 1173-1176.
32. Sonoda, J. and Wharton, R.P. (1999) Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev., 13, 2704-2712.
33. Sonoda, J. and Wharton, R.P. (2001) Drosophila Brain Tumor is a translational repressor. Genes Dev., 15, 762-773.
34. Sosnowski, B.A., Belote, J.M. and McKeown, M. (1989) Sex-specific alternative splicing of RNA from the transformer gene results from sequence-dependent splice site blockage. Cell, 58, 449-459.
35. Stripecke, R. and Hentze, M.W. (1992) Bacteriophage and spliceosomal proteins function as position-dependent cis/trans repressors of mRNA translation in vitro. Nucleic Acids Res., 20, 5555-5564.
36. Stripecke, R., Oliveira, C.C., McCarthy, J.E. and Hentze, M.W. (1994) Proteins binding to 5′ untranslated region sites: a general mechanism for translational regulation of mRNAs in human and yeast cells. Mol. Cell. Biol., 14, 5898-5909.
37. Tan, R. and Frankel, A.D. (1995) Structural variety of arginine-rich RNA-binding peptides. Proc. Natl Acad. Sci. USA, 92, 5282-5286.
38. Valcárcel, J., Singh, R., Zamore, P.D. and Green, M.R. (1993) The protein Sex-lethal antagonizes the splicing factor U2AF to regulate alternative splicing of transformer pre-mRNA. Nature, 362, 171-175.
39. Wang, J. and Bell, L.R. (1994) The Sex-lethal amino terminus mediates cooperative interactions in RNA binding and is essential for splicing regulation. Genes Dev., 8, 2072-2085.
40. Wang, J., Dong, Z. and Bell, L.R. (1997) Sex-lethal interactions with protein and RNA. Roles of glycine-rich and RNA binding domains. J. Biol. Chem., 272, 22227-22235.
41. Wharton, R.P., Sonoda, J., Lee, T., Patterson, M. and Murata, Y. (1998) The Pumilio RNA-binding domain is also a translational regulator. Mol. Cell, 1, 863-872.
42. Wickens, M., Bernstein, D.S., Kimble, J. and Parker, R. (2002) A PUF family portrait: 3′UTR regulation as a way of life. Trends Genet., 18, 150-157.
43. Wilkinson, M.F. and Shyu, A.B. (2001) Multifunctional regulatory proteins that control gene expression in both the nucleus and the cytoplasm. BioEssays, 23, 775-787.
44. Yanowitz, J.L., Deshpande, G., Calhoun, G. and Schedl, P.D. (1999) An N-terminal truncation uncouples the sex-transforming and dosage compensation functions of sex-lethal. Mol. Cell. Biol., 19, 3018-3028.