NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1

Nature Structural and Molecular Biology

Volumn 17, Issue 11, 2010, Pages 1367-1376

  Güttler, Thomas ^a   Madl, Tobias ^b,c   Neumann, Piotr ^d   Deichsel, Danilo ^a   Corsini, Lorenzo ^b,c   Monecke, Thomas ^d   Ficner, Ralf ^d   Sattler, Michael ^b,c   Görlich, Dirk ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; EXPORTIN 1; GUANOSINE TRIPHOSPHATE; PROLINE; RAN PROTEIN; REV PROTEIN;

ALPHA HELIX; ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ACTIVE TRANSPORT, CELL NUCLEUS; BINDING SITES; CONSENSUS SEQUENCE; CRYSTALLOGRAPHY, X-RAY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KARYOPHERINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR EXPORT SIGNALS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY; RAN GTP-BINDING PROTEIN; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 78549264393     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1931     Document Type: Article

References (65)

1. Görlich, D. & Kutay, U. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15, 607-660 (1999).
2. Cook, A.G. & Conti, E. Nuclear export complexes in the frame. Curr. Opin. Struct. Biol. 20, 247-252 (2010).
3. Adachi, Y. & Yanagida, M. Higher order chromosome structure is affected by cold-sensitive mutations in a Schizosaccharomyces pombe gene crm1+ which encodes a 115-kD protein preferentially localized in the nucleus and its periphery. J. Cell Biol. 108, 1195-1207 (1989).
4. Fornerod, M., Ohno, M., Yoshida, M. & Mattaj, I.W. Crm1 is an export receptor for leucine rich nuclear export signals. Cell 90, 1051-1060 (1997).
5. Stade, K., Ford, C.S., Guthrie, C. & Weis, K. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90, 1041-1050 (1997).
6. Nishi, K. et al. Leptomycin B targets a regulatory cascade of crm1, a fssion yeast nuclear protein, involved in control of higher order chromosome structure and gene expression. J. Biol. Chem. 269, 6320-6324 (1994).
7. Wolff, B., Sanglier, J.J. & Wang, Y. Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodefciency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem. Biol. 4, 139-147 (1997).
8. Kutay, U., Bischoff, F.R., Kostka, S., Kraft, R. & Görlich, D. Export of importin alpha from the nucleus is mediated by a specifc nuclear transport factor. Cell 90, 1061-1071 (1997).
9. Matsuura, Y. & Stewart, M. Structural basis for the assembly of a nuclear export complex. Nature 432, 872-877 (2004).
10. Cook, A.G., Fukuhara, N., Jinek, M. & Conti, E. Structures of the tRNA export factor in the nuclear and cytosolic states. Nature 461, 60-65 (2009).
11. Okada, C. et al. A high-resolution structure of the pre-microRNA nuclear export machinery. Science 326, 1275-1279 (2009).
12. Monecke, T. et al. Crystal Structure of the Nuclear Export Receptor CRM1 in Complex with Snurportin1 and RanGTP. Science 324, 1087-1091 (2009).
13. Dong, X. et al. Structural basis for leucine-rich nuclear export signal recognition by CRM1. Nature 458, 1136-1141 (2009).
14. Koyama, M. & Matsuura, Y. An allosteric mechanism to displace nuclear export cargo from CRM1 and RanGTP by RanBP1. EMBO J. 29, 2002-2013 (2010).
15. Ho, J.H., Kallstrom, G. & Johnson, A.W. Nmd3p is a Crm1p-dependent adapter protein for nuclear export of the large ribosomal subunit. J. Cell Biol. 151, 1057-1066 (2000).
16. Gadal, O. et al. Nuclear export of 60s ribosomal subunits depends on Xpo1p and requires a nuclear export sequence-containing factor, Nmd3p, that associates with the large subunit protein Rpl10p. Mol. Cell. Biol. 21, 3405-3415 (2001).
17. Moy, T.I. & Silver, P.A. Requirements for the nuclear export of the small ribosomal subunit. J. Cell Sci. 115, 2985-2995 (2002).
18. Thomas, F. & Kutay, U. Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway. J. Cell Sci. 116, 2409-2419 (2003).
19. Malim, M.H., McCarn, D.F., Tiley, L.S. & Cullen, B.R. Mutational defnition of the human immunodefciency virus type 1 Rev activation domain. J. Virol. 65, 4248-4254 (1991).
20. Fischer, U., Huber, J., Boelens, W.C., Mattaj, I.W. & Lührmann, R. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specifc cellular RNAs. Cell 82, 475-483 (1995).
21. Wen, W., Meinkoth, J., Tsien, R. & Taylor, S. Identifcation of a signal for rapid export of proteins from the nucleus. Cell 82, 463-473 (1995).
22. Bohnsack, M.T. et al. Exp5 exports eEF1A via tRNA from nuclei and synergizes with other transport pathways to confne translation to the cytoplasm. EMBO J. 21, 6205-6215 (2002).
23. Richards, S.A., Lounsbury, K.M., Carey, K.L. & Macara, I.G. A nuclear export signal is essential for the cytosolic localization of the Ran binding protein, RanBP1. J. Cell Biol. 134, 1157-1168 (1996).
24. Izaurralde, E., Kutay, U., von Kobbe, C., Mattaj, I.W. & Görlich, D. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J. 16, 6535-6547 (1997).
25. Kutay, U. & Guttinger, S. Leucine-rich nuclear-export signals: born to be weak. Trends Cell Biol. 15, 121-124 (2005).
26. Bogerd, H.P., Fridell, R.A., Benson, R.E., Hua, J. & Cullen, B.R. Protein sequence requirements for function of the human T-cell leukemia virus type 1 Rex nuclear export signal delineated by a novel in vivo randomization-selection assay. Mol. Cell. Biol. 16, 4207-4214 (1996).
27. Zhang, M.J. & Dayton, A.I. Tolerance of diverse amino acid substitutions at conserved positions in the nuclear export signal (NES) of HIV-1 Rev. Biochem. Biophys. Res. Commun. 243, 113-116 (1998).
28. Kosugi, S., Hasebe, M., Tomita, M. & Yanagawa, H. Nuclear export signal consensus sequences defned using a localization-based yeast selection system. Traffc 9, 2053-2062 (2008).
29. Huber, J. et al. Snurportin1, an m3G-cap-specifc nuclear import receptor with a novel domain structure. EMBO J. 17, 4114-4126 (1998).
30. Paraskeva, E. et al. CRM1-mediated recycling of snurportin 1 to the cytoplasm. J. Cell Biol. 145, 255-264 (1999).
31. Engelsma, D., Bernad, R., Calafat, J. & Fornerod, M. Supraphysiological nuclear export signals bind CRM1 independently of RanGTP and arrest at Nup358. EMBO J. 23, 3643-3652 (2004).
32. Engelsma, D. et al. A supraphysiological nuclear export signal is required for parvovirus nuclear export. Mol. Biol. Cell 19, 2544-2552 (2008).
33. Cook, A., Bono, F., Jinek, M. & Conti, E. Structural biology of nucleocytoplasmic transport. Annu. Rev. Biochem. 76, 647-671 (2007).
34. Rice, L.M. & Brunger, A.T. Torsion angle dynamics: reduced variable conformational sampling enhances crystallographic structure refnement. Proteins 19, 277-290 (1994).
35. Kudo, N. et al. Leptomycin B inactivates CRM1/exportin 1 by covalent modifcation at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. USA 96, 9112-9117 (1999).
36. Nilges, M. A calculation strategy for the structure determination of symmetrical dimers by H-1-NMR. Proteins 17, 297-309 (1993).
37. Nilges, M. & O'Donoghue, S.I. Ambiguous NOEs and automated NOE assignment. Prog. Nucl. Magn. Reson. Spectrosc. 32, 107-139 (1998).
38. Madl, T., Bermel, W. & Zangger, K. Use of relaxation enhancements in a paramagnetic environment for the structure determination of proteins using NMR spectroscopy. Angew. Chem. Int. Ed. 48, 8259-8262 (2009).
39. Askjaer, P. et al. RanGTP-regulated interactions of CRM1 with nucleoporins and a shuttling DEAD-box helicase. Mol. Cell. Biol. 19, 6276-6285 (1999).
40. Hantschel, O. et al. Structural basis for the cytoskeletal association of Bcr-Abl/c-Abl. Mol. Cell 19, 461-473 (2005).
41. Taagepera, S. et al. Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proc. Natl. Acad. Sci. USA 95, 7457-7462 (1998).
42. Hutchinson, E.G. & Thornton, J.M. PROMOTIF-a program to identify and analyze structural motifs in proteins. Protein Sci. 5, 212-220 (1996).
43. Ribbeck, K. & Görlich, D. The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J. 21, 2664-2671 (2002).
44. Weiss, M.S. & Hilgenfeld, R. On the use of the merging R factor as a quality indicator for X-ray data. J. Appl. Cryst. 30, 203-205 (1997).
45. Linge, J.P., Williams, M.A., Spronk, C.A., Bonvin, A.M. & Nilges, M. Refnement of protein structures in explicit solvent. Proteins 50, 496-506 (2003).
46. Shen, Y., Delaglio, F., Cornilescu, G. & Bax, A. TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223 (2009).
47. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R. & Thornton, J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (1996).
48. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Cryst. 26, 795-800 (1993).
49. Brunger, A.T. Version 1.2 of the Crystallography and NMR system. Nat. Protoc. 2, 2728-2733 (2007).
50. Adams, P.D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954 (2002).
51. McCoy, A.J. Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr. 63, 32-41 (2007).
52. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
53. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
54. Riek, R., Wider, G., Pervushin, K. & Wüthrich, K. Polarization transfer by cross-correlated relaxation in solution NMR with very large molecules. Proc. Natl. Acad. Sci. USA 96, 4918-4923 (1999).
55. Tugarinov, V., Hwang, P.M., Ollerenshaw, J.E. & Kay, L.E. Cross-correlated relaxation enhanced 1H[bond]13C NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes. J. Am. Chem. Soc. 125, 10420-10428 (2003).
56. 13C-detected protonless NMR spectroscopy of proteins in solution. Prog. Nucl. Magn. Reson. Spectrosc. 48, 25-45 (2006).
57. Oh, B.H., Westler, W.M., Darba, P. & Markley, J.L. Protein C-13 spin systems by a single two-dimensional nuclear magnetic-resonance experiment. Science 240, 908-911 (1988).
58. Delaglio, F. et al. Nmrpipe-a multidimensional spectral processing system based on unix pipes. J. Biomol. NMR 6, 277-293 (1995).
59. Johnson, B.A. & Blevins, R.A. NMRView: a computer-program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614 (1994).
60. Pintacuda, G. & Otting, G. Identifcation of protein surfaces by NMR measurements with a paramagnetic Gd(III) chelate. J. Am. Chem. Soc. 124, 372-373 (2002).
61. Linge, J.P., Habeck, M., Rieping, W. & Nilges, M. ARIA: automated NOE assignment and NMR structure calculation. Bioinformatics 19, 315-316 (2003).
62. Linge, J.P., O'Donoghue, S.I. & Nilges, M. Automated assignment of ambiguous nuclear overhauser effects with ARIA. Methods Enzymol. 339, 71-90 (2001).
63. Adam, S.A., Marr, R.S. & Gerace, L. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111, 807-816 (1990).
64. Stüven, T., Hartmann, E. & Görlich, D. Exportin 6: a novel nuclear export receptor that is specifc for proflin.actin complexes. EMBO J. 22, 5928-5940 (2003).
65. Leno, G.H. & Laskey, R.A. DNA replication in cell-free extracts from Xenopus laevis. Methods Cell Biol. 36, 561-579 (1991).