The Crystal Structure of Mouse Nup35 Reveals Atypical RNP Motifs and Novel Homodimerization of the RRM Domain

Journal of Molecular Biology

Volumn 363, Issue 1, 2006, Pages 114-124

  Handa, Noriko ^a   Kukimoto Niino, Mutsuko ^a   Akasaka, Ryogo ^a   Kishishita, Seiichiro ^a   Murayama, Kazutaka ^a,b   Terada, Takaho ^a   Inoue, Makoto ^a   Kigawa, Takanori ^a,c   Kose, Shingo ^d   Imamoto, Naoko ^d   Tanaka, Akiko ^a   Hayashizaki, Yoshihide ^a   Shirouzu, Mikako ^a   Yokoyama, Shigeyuki ^a,e  

^a RIKEN YOKOHAMA INSTITUTE   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^d Japan Science and Technology Agency   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

homodimer; NPC; nuclear pore protein; Nup35; RRM domain

Indexed keywords

HOMODIMER; METHIONINE; MONOMER; NUP35 PROTEIN; PHENYLALANINE; PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; CRYSTAL STRUCTURE; DIMERIZATION; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; ULTRACENTRIFUGATION;

SACCHAROMYCES CEREVISIAE; VERTEBRATA;

EID: 33748799705     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.07.089     Document Type: Article

References (56)

1. Weis K. Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 112 (2003) 441-451
2. Fahrenkrog B., and Aebi U. The nuclear pore complex: nucleocytoplasmic transport and beyond. Nature Rev. Mol. Cell Biol. 4 (2003) 757-766
3. Suntharalingam M., and Wente S.R. Peering through the pore: nuclear pore complex structure, assembly, and function. Dev. Cell 4 (2003) 775-789
4. Rout M.P., Aitchison J.D., Suprapto A., Hjertaas K., Zhao Y., and Chait B.T. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148 (2000) 635-651
5. Cronshaw J.M., Krutchinsky A.N., Zhang W., Chait B.T., and Matunis M.J. Proteomic analysis of the mammalian nuclear pore complex. J. Cell Biol. 158 (2002) 915-927
6. Pemberton L.F., and Paschal B.M. Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6 (2005) 187-198
7. Ryan K.J., and Wente S.R. The nuclear pore complex: a protein machine bridging the nucleus and cytoplasm. Curr. Opin. Cell Biol. 12 (2000) 361-371
8. Makhnevych T., Lusk C.P., Anderson A.M., Aitchison J.D., and Wozniak R.W. Cell cycle regulated transport controlled by alterations in the nuclear pore complex. Cell 115 (2003) 813-823
9. Lusk C.P., Makhnevych T., Marelli M., Aitchison J.D., and Wozniak R.W. Karyopherins in nuclear pore biogenesis: a role for Kap121p in the assembly of Nup53p into nuclear pore complexes. J. Cell Biol. 159 (2002) 267-278
10. Scott R.J., Lusk C.P., Dilworth D.J., Aitchison J.D., and Wozniak R.W. Interactions between Mad1p and the nuclear transport machinery in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 16 (2005) 4362-4374
11. Hawryluk-Gara L.A., Shibuya E.K., and Wozniak R.W. Vertebrate Nup53 interacts with the nuclear lamina and is required for the assembly of a Nup93-containing complex. Mol. Biol. Cell 16 (2005) 2382-2394
12. Devos D., Dokudovskaya S., Williams R., Alber F., Eswar N., Chait B.T., et al. Simple fold composition and modular architecture of the nuclear pore complex. Proc. Natl Acad. Sci. USA 103 (2006) 2172-2177
13. Marelli M., Lusk C.P., Chan H., Aitchison J.D., and Wozniak R.W. A link between the synthesis of nucleoporins and the biogenesis of the nuclear envelope. J. Cell Biol. 153 (2001) 709-724
14. Mansfeld J., Guttinger S., Hawryluk-Gara L.A., Pante N., Mall M., Galy V., et al. The conserved transmembrane nucleoporin NDC1 is required for nuclear pore complex assembly in vertebrate cells. Mol. Cell 22 (2006) 93-103
15. Birney E., Kumar S., and Krainer A.R. Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucl. Acids Res. 21 (1993) 5803-5816
16. Burd C.G., and Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science 265 (1994) 615-621
17. Maris C., Dominguez C., and Allain F.H. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J. 272 (2005) 2118-2131
18. Varani G., and Nagai K. RNA recognition by RNP proteins during RNA processing. Annu. Rev. Biophys. Biomol. Struct. 27 (1998) 407-445
19. Varani L., Gunderson S.I., Mattaj I.W., Kay L.E., Neuhaus D., and Varani G. The NMR structure of the 38 kDa U1A protein - PIE RNA complex reveals the basis of cooperativity in regulation of polyadenylation by human U1A protein. Nature Struct. Biol. 7 (2000) 329-335
20. Shamoo Y., Krueger U., Rice L.M., Williams K.R., and Steitz T.A. Crystal structure of the two RNA binding domains of human hnRNP A1 at 1.75 Å resolution. Nature Struct. Biol. 4 (1997) 215-222
21. Xu R.M., Jokhan L., Cheng X., Mayeda A., and Krainer A.R. Crystal structure of human UP1, the domain of hnRNP A1 that contains two RNA-recognition motifs. Structure 5 (1997) 559-570
22. Handa N., Nureki O., Kurimoto K., Kim I., Sakamoto H., Shimura Y., et al. Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature 398 (1999) 579-585
23. Wang X., and Tanaka Hall T.M. Structural basis for recognition of AU-rich element RNA by the HuD protein. Nature Struct. Biol. 8 (2001) 141-145
24. Deo R.C., Bonanno J.B., Sonenberg N., and Burley S.K. Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell 98 (1999) 835-845
25. Price S.R., Evans P.R., and Nagai K. Crystal structure of the spliceosomal U2B″-U2A′ protein complex bound to a fragment of U2 small nuclear RNA. Nature 394 (1998) 645-650
26. Mazza C., Ohno M., Segref A., Mattaj I.W., and Cusack S. Crystal structure of the human nuclear cap binding complex. Mol. Cell 8 (2001) 383-396
27. Fribourg S., Gatfield D., Izaurralde E., and Conti E. A novel mode of RBD-protein recognition in the Y14-Mago complex. Nature Struct. Biol. 10 (2003) 433-439
28. Lau C.K., Diem M.D., Dreyfuss G., and Van Duyne G.D. Structure of the Y14-Magoh core of the exon junction complex. Curr. Biol. 13 (2003) 933-941
29. Bono F., Ebert J., Unterholzner L., Guttler T., Izaurralde E., and Conti E. Molecular insights into the interaction of PYM with the Mago-Y14 core of the exon junction complex. EMBO Rep. 5 (2004) 304-310
30. Kadlec J., Izaurralde E., and Cusack S. The structural basis for the interaction between nonsense-mediated mRNA decay factors UPF2 and UPF3. Nature Struct. Mol. Biol. 11 (2004) 330-337
31. Kielkopf C.L., Rodionova N.A., Green M.R., and Burley S.K. A novel peptide recognition mode revealed by the X-ray structure of a core U2AF35/U2AF65 heterodimer. Cell 106 (2001) 595-605
32. Selenko P., Gregorovic G., Sprangers R., Stier G., Rhani Z., Kramer A., and Sattler M. Structural basis for the molecular recognition between human splicing factors U2AF65 and SF1/mBBP. Mol. Cell 11 (2003) 965-976
33. Kielkopf C.L., Lucke S., and Green M.R. U2AF homology motifs: protein recognition in the RRM world. Genes Dev. 18 (2004) 1513-1526
34. Schellenberg M.J., Edwards R.A., Ritchie D.B., Kent O.A., Golas M.M., Stark H., et al. Crystal structure of a core spliceosomal protein interface. Proc. Natl Acad. Sci. USA 103 (2006) 1266-1271
35. Carninci P., Waki K., Shiraki T., Konno H., Shibata K., Itoh M., et al. Targeting a complex transcriptome: the construction of the mouse full-length cDNA encyclopedia. Genome Res. 13 (2003) 1273-1289
36. Nagai K., Oubridge C., Jessen T.H., Li J., and Evans P.R. Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A. Nature 348 (1990) 515-520
37. Oubridge C., Ito N., Teo C.H., Fearnley I., and Nagai K. Crystallisation of RNA-protein complexes. II. The application of protein engineering for crystallisation of the U1A protein-RNA complex. J. Mol. Biol. 249 (1995) 409-423
38. Holm L., and Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233 (1993) 123-138
39. Marelli M., Aitchison J.D., and Wozniak R.W. Specific binding of the karyopherin Kap121p to a subunit of the nuclear pore complex containing Nup53p, Nup59p, and Nup170p. J. Cell Biol. 143 (1998) 1813-1830
40. Inoue M., Muto Y., Sakamoto H., Kigawa T., Takio K., Shimura Y., and Yokoyama S. A characteristic arrangement of aromatic amino acid residues in the solution structure of the amino-terminal RNA-binding domain of Drosophila sex-lethal. J. Mol. Biol. 272 (1997) 82-94
41. Strawn L.A., Shen T., Shulga N., Goldfarb D.S., and Wente S.R. Minimal nuclear pore complexes define FG repeat domains essential for transport. Nature Cell Biol. 6 (2004) 197-206
42. Denning D.P., Patel S.S., Uversky V., Fink A.L., and Rexach M. Disorder in the nuclear pore complex: the FG repeat regions of nucleoporins are natively unfolded. Proc. Natl Acad. Sci. USA 100 (2003) 2450-2455
43. Kigawa T., Yabuki T., Matsuda N., Matsuda T., Nakajima R., Tanaka A., and Yokoyama S. Preparation of Escherichia coli cell extract for highly productive cell-free protein expression. J. Struct. Funct. Genomics 5 (2004) 63-68
44. Wada T., Shirouzu M., Terada T., Ishizuka Y., Matsuda T., Kigawa T., et al. Structure of a conserved CoA-binding protein synthesized by a cell-free system. Acta Crystallog. sect. D 59 (2003) 1213-1218
45. Kigawa T., Yabuki T., and Yokoyama S. Large-scale protein preparation using the cell-free synthesis. Tanpakushitsu Kakusan Koso 44 (1999) 598-605
46. Kigawa T., Yabuki T., Yoshida Y., Tsutsui M., Ito Y., Shibata T., and Yokoyama S. Cell-free production and stable-isotope labeling of milligram quantities of proteins. FEBS Letters 442 (1999) 15-19
47. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
48. Terwilliger T.C., and Berendzen J. Automated MAD and MIR structure solution. Acta Crystallog. sect. D 55 (1999) 849-861
49. Terwilliger T. SOLVE and RESOLVE: automated structure solution, density modification and model building. J. Synchrotron Radiat. 11 (2004) 49-52
50. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
51. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291
52. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24 (1991) 946-950
53. Merritt E.A., and Murphy M.E. Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallog. sect. D 50 (1994) 869-873
54. Kenan D.J., Query C.C., and Keene J.D. RNA recognition: towards identifying determinants of specificity. Trends Biochem. Sci. 16 (1991) 214-220
55. Gouet P., Courcelle E., Stuart D.I., and Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15 (1999) 305-308
56. Glaser F., Pupko T., Paz I., Bell R.E., Bechor-Shental D., Martz E., and Ben-Tal N. ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 19 (2003) 163-164