Structural basis for the assembly of the Sxl-Unr translation regulatory complex

Nature

Volumn 515, Issue 7526, 2014, Pages 287-290

  Hennig, Janosch ^a,b   Militti, Cristina ^c,d   Popowicz, Grzegorz M ^a,b   Wang, Iren ^a,b   Sonntag, Miriam ^a,b   Geerlof, Arie ^a   Gabel, Frank ^e,f,g,h   Gebauer, Fátima ^c,d   Sattler, Michael ^a,b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b Munich Center for Integrated Protein Science   (Germany)

^c CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^d UNIVERSITAT POMPEU FABRA   (Spain)

^e UNIV GRENOBLE ALPES   (France)

^f CNRS   (France)

^g INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^h INSTITUT LAUE LANGEVIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COLD SHOCK PROTEIN; PROTEIN; RIBONUCLEOPROTEIN; RNA; SEX LETHAL PROTEIN; UNCLASSIFIED DRUG; UPSTREAM OF N RAS PROTEIN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; MESSENGER RNA; RNA BINDING PROTEIN; SXL PROTEIN, DROSOPHILA; UNR PROTEIN, DROSOPHILA;

CHROMOSOME; CRYSTAL STRUCTURE; FLY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC DIFFERENTIATION; PROTEIN; RNA; VIABILITY;

ALPHA HELIX; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; NEUTRON SCATTERING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; RADIATION SCATTERING; RNA BINDING; RNA TRANSLATION; ANIMAL; BINDING SITE; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; COLD SHOCK RESPONSE; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; NEUTRON DIFFRACTION; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE MOTIF; PROTEIN SYNTHESIS; PROTEIN TERTIARY STRUCTURE; SMALL ANGLE SCATTERING; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

DROSOPHILA MELANOGASTER;

ANIMALS; BINDING SITES; CELL LINE; COLD-SHOCK RESPONSE; CRYSTALLOGRAPHY, X-RAY; DNA-BINDING PROTEINS; DOSAGE COMPENSATION, GENETIC; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION; MALE; MODELS, MOLECULAR; NEUTRON DIFFRACTION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEOTIDE MOTIFS; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS; SCATTERING, SMALL ANGLE; STRUCTURE-ACTIVITY RELATIONSHIP; X-RAY DIFFRACTION;

EID: 84920606340     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13693     Document Type: Article

References (60)

1. Conrad, T.&Akhtar, A.Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nature Rev.Genet.13, 123-134(2012).
2. Gelbart, M. E. & Kuroda, M. I. Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136, 1399-1410 (2009).
3. Graindorge, A., Militti, C. & Gebauer, F. Posttranscriptional control of X-chromosome dosage compensation. Wiley Interdiscip. Rev. RNA 2, 534-545 (2011).
4. Beckmann, K., Grskovic, M., Gebauer, F. & Hentze, M. W. A dual inhibitory mechanism restricts msl-2 mRNA translation for dosage compensation in Drosophila. Cell 122, 529-540 (2005).
5. Abaza, I., Coll, O., Patalano, S. & Gebauer, F. Drosophila UNR is required for translational repression of male-specific lethal 2 mRNA during regulation of X-chromosome dosage compensation. Genes Dev. 20, 380-389 (2006).
6. Duncan, K. et al. Sex-lethalimparts a sex-specific function toUNRby recruiting it to the msl-2mRNA39 UTR: translational repression for dosage compensation. Genes Dev. 20, 368-379 (2006).
7. Grskovic, M., Hentze, M. W. & Gebauer, F. A co-repressor assembly nucleated by Sex-lethal in the 39UTR mediates translational control of Drosophila msl-2 mRNA. EMBO J. 22, 5571-5581 (2003).
8. Schindelin, H., Marahiel, M. A. & Heinemann, U. Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature 364, 164-168 (1993).
9. Abaza, I. & Gebauer, F. Functional domains of Drosophila UNR in translational control. RNA 14, 482-490 (2008).
10. Gebauer, F., Grskovic, M. & Hentze, M. W. Drosophila sex-lethal inhibits the stable association of the 40S ribosomal subunit with msl-2 mRNA. Mol. Cell 11, 1397-1404 (2003).
11. Handa, N. et al. Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature 398, 579-585 (1999).
12. Sachs, R., Max, K. E., Heinemann, U. & Balbach, J. RNA single strands bind to a conservedsurface of the major cold shock protein in crystalsand solution.RNA18, 65-76 (2012).
13. Mayr, F., Schutz, A., Doge, N. & Heinemann, U. The Lin28 cold-shock domain remodels pre-let-7 microRNA. Nucleic Acids Res. 40, 7492-7506 (2012).
14. Nam, Y., Chen, C., Gregory, R. I., Chou, J. J.&Sliz, P.Molecular basis for interactionof let-7 microRNAs with Lin28. Cell 147, 1080-1091 (2011).
15. McLaughlin, K. J., Jenkins, J. L. & Kielkopf, C. L. Large favorable enthalpy changes drive specificRNArecognition byRNA recognitionmotif proteins. Biochemistry 50, 1429-1431 (2011).
16. Cline, T. W.Autoregulatory functioningofaDrosophila geneproduct that establishes and maintains the sexually determined state. Genetics 107, 231-277 (1984).
17. Bernstein, M., Lersch, R. A., Subrahmanyan, L.& Cline, T. W. Transposon insertions causing constitutive Sex-lethal activity in Drosophila melanogaster affect Sxl sexspecific transcript splicing. Genetics 139, 631-648 (1995).
18. Maine, E. M., Salz, H. K., Cline, T. W. & Schedl, P. The Sex-lethal gene of Drosophila: DNA alterations associated with sex-specific lethal mutations. Cell 43, 521-529 (1985).
19. Valcárcel, J., Singh, R., Zamore, P. D. & Green, M. R. The protein Sex-lethal antagonizes the splicing factorU2AF to regulate alternative splicing of transformer pre-mRNA. Nature 362, 171-175 (1993).
20. Triqueneaux, G., Velten, M., Franzon, P., Dautry, F. & Jacquemin-Sablon, H. RNA binding specificity of Unr, a protein with five cold shock domains. Nucleic Acids Res. 27, 1926-1934 (1999).
21. Drosophila 12 Genomes Consortium. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450, 203-218 (2007).
22. Park, S. W. et al. An evolutionarily conserved domain of roX2 RNA is sufficient for induction ofH4-Lys16 acetylation on the Drosophila X chromosome. Genetics 177, 1429-1437 (2007).
23. Weber, G., Trowitzsch, S., Kastner, B., Luhrmann, R. & Wahl, M. C. Functional organization of the Smcore in the crystal structure of human U1 snRNP. EMBO J. 29, 4172-4184 (2010).
24. Pomeranz Krummel, D. A., Oubridge, C., Leung, A. K., Li, J. & Nagai, K. Crystal structure of human spliceosomal U1 snRNP at 5.5A° resolution. Nature 458, 475-480 (2009).
25. Bono, F., Ebert, J., Lorentzen, E.&Conti, E. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell 126, 713-725 (2006).
26. Mackereth, C. D. et al.Multi-domain conformational selection underlies pre-mRNA splicing regulation by U2AF. Nature 475, 408-411 (2011).
27. Mackereth, C. D. & Sattler, M. Dynamics in multi-domain protein recognition of RNA. Curr. Opin. Struct. Biol. 22, 287-296 (2012).
28. Baltz, A. G. et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol. Cell 46, 674-690 (2012).
29. Castello, A. et al. Insights into RNA biology from an atlas of mammalian mRNAbinding proteins. Cell 149, 1393-1406 (2012).
30. Hennig, J., Wang, I., Sonntag, M., Gabel, F. & Sattler, M. Combining NMR and small angle X-ray and neutron scattering in the structural analysis of a ternary protein-RNA complex. J. Biomol. NMR 56, 17-30 (2013).
31. Wen, J., Arakawa, T. & Philo, J. S. Size-exclusion chromatography with on-line light-scattering, absorbance, and refractive index detectors for studying proteins and their interactions. Anal. Biochem. 240, 155-166 (1996).
32. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Cryst. 40, 658-674 (2007).
33. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
34. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
35. Winn, M. D., Murshudov, G. N. & Papiz, M. Z. Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol. 374, 300-321 (2003).
36. Gebauer, F., Corona, D. F., Preiss, T., Becker, P. B. & Hentze, M. W. Translational control of dosage compensation in Drosophila by Sex-lethal: cooperative silencing via the 59 and 39 UTRs of msl-2 mRNA is independent of the poly(A) tail. EMBO J. 18, 6146-6154 (1999).
37. Sattler, M., Schleucher, J. & Griesinger, C. Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. Nucl. Magn. Reson. Spectrosc. 34, 93-158 (1999).
38. Salzmann, M., Pervushin, K., Wider, G., Senn, H. & Wuthrich, K. [13C]-constanttime [15N, 1H]-TROSY-HNCA for sequential assignments of large proteins. J. Biomol. NMR 14, 85-88 (1999).
39. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing systembased on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
40. Goddard, T. D. & Kneller, D. G. SPARKY 3. (Univ. California)
41. Cordier, F., Dingley, A. J. & Grzesiek, S. A doublet-separated sensitivity-enhanced HSQC for the determination of scalar and dipolar one-bond J-couplings. J. Biomol. NMR 13, 175-180 (1999).
42. Yang, D. & Kay, L. E. Improved 1HN-detected triple resonance TROSY-based experiments. J. Biomol. NMR 13, 3-10 (1999).
43. Otting, G., Ruckert, M., Levitt, M. H. & Moshref, A. NMR experiments for the sign determination of homonuclear scalar and residual dipolar couplings. J. Biomol. NMR 16, 343-346 (2000).
44. Dosset, P., Hus, J. C., Marion, D. & Blackledge, M. A novel interactive tool for rigid-body modeling of multi-domain macromolecules using residual dipolar couplings. J. Biomol. NMR 20, 223-231 (2001).
45. Gosh, R. E. et al. A computing guide forsmall-angle scattering. ILL Technical Report ILL06GH05T. (2006).
46. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. & Svergun, D. I. PRIMUS: a Windows-PC based system for small-angle scattering data analysis. J. Appl. Cryst. 36, 1277-1282 (2003).
47. Svergun, D. I., Barberato, C. & Koch, M. H. J. CRYSOL-a program to evaluate x-ray solution scattering of biologicalmacromolecules fromatomic coordinates. J. Appl. Cryst. 28, 768-773 (1995).
48. Svergun, D. I. et al. Protein hydration in solution: experimental observation by x-ray and neutron scattering. Proc. Natl Acad. Sci. USA 95, 2267-2272 (1998).
49. Svergun, D. I. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-2886 (1999).
50. Svergun, D. I. Determination of the regularization parameter in indirect-transform methods using preceptual criteria. J. Appl. Cryst. 25, 495-503 (1992).
51. Volkov, V. V. & Svergun, D. I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Cryst. 36, 860-864 (2003).
52. Kozin, M. & Svergun, D. I. Automated matching of high-and low-resolution structural models. J. Appl. Cryst. 34, 33-41 (2001).
53. Jacrot, B. Study of biological structures by neutron-scattering from solution. Rep. Prog. Phys. 39, 911-953 (1976).
54. Voss, N. R. & Gerstein, M. Calculation of standard atomic volumes for RNA and comparison with proteins: RNA is packed more tightly. J. Mol. Biol. 346, 477-492 (2005).
55. Cornilescu, G., Marquardt, J. L., Ottiger, M. & Bax, A. Validation of protein structure fromanisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J. Am. Chem. Soc. 120, 6836-6837 (1998).
56. Gouet, P., Courcelle, E., Stuart, D. I. & Metoz, F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (1999).
57. St Pierre, S. E., Ponting, L., Stefancsik, R., McQuilton, P. & the FlyBase Consortium. FlyBase 102-advanced approaches to interrogating FlyBase. Nucleic Acids Res. 42, D780-D788 (2014).
58. Sievers, F. et al. Fast, scalable generation of high-quality proteinmultiple sequence alignments using Clustal Omega. Mol. Syst. Biol. http://dx.doi.org/10.1038/msb.2011.75 (11 November 2011).
59. Dereeper, A. et al.Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465-W469 (2008).
60. Jacques, D. A., Guss, J. M., Svergun, D. I. & Trewhella, J. Publication guidelines for structural modelling of small-angle scattering data frombiomolecules in solution. Acta Crystallogr. D 68, 620-626 (2012).