Structural determinants of nuclear export signal orientation in binding to exportin CRM1

eLife

Volumn 4, Issue September 2015, 2015, Pages

  Fung, Ho Yee Joyce ^a   Fu, Szu Chin ^a   Brautigam, Chad A ^b   Chook, Yuh Min ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; PROTEOME; CELL RECEPTOR; EXPORTIN 1 PROTEIN; KARYOPHERIN; NUCLEAR EXPORT SIGNAL; PROTEIN BINDING;

AFFINITY CHROMATOGRAPHY; ARTICLE; BINDING AFFINITY; BINDING ASSAY; BIOCHEMICAL ANALYSIS; BIOINFORMATICS; BLEACHING; COMPLEX FORMATION; CRYSTALLIZATION; GEL PERMEATION CHROMATOGRAPHY; HUMAN; ION EXCHANGE CHROMATOGRAPHY; MASS SPECTROMETRY; MUTAGENESIS; NUCLEAR EXPORT SIGNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; HUMANS; KARYOPHERINS; MODELS, MOLECULAR; NUCLEAR EXPORT SIGNALS; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84943807571     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10034     Document Type: Article

References (49)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica. Section D, Biological Crystallography 66:213-221. doi: 10.1107/S0907444909052925.
2. Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, Terwilliger TC, Urzhumtsev A, Zwart PH, Adams PD. 2012. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallographica. Section D, Biological Crystallography 68:352-367. doi: 10.1107/S0907444912001308.
3. Akopian D, Shen K, Zhang X, Shan SO. 2013. Signal recognition particle: an essential protein-targeting machine. Annual Review of Biochemistry 82:693-721. doi: 10.1146/annurev-biochem-072711-164732.
4. Bevington PR, Robinson DK. 1992. Data reduction and error analysis for the physical sciences. New York: Mc-Graw-Hill.
5. Brautigam CA. 2015. Calculations and publication-quality illustrations for analytical ultracentrifugation data. Methods in Enzymology 562:109-133. doi: 10.1016/bs.mie.2015.05.001.
6. Chen VB, Arendall WB III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica. Section D, Biological Crystallography 66:12-21. doi: 10.1107/S0907444909042073.
7. Chook YM, Blobel G. 1999. Structure of the nuclear transport complex karyopherin-beta2-Ran x GppNHp. Nature 399:230-237. doi: 10.1038/20375.
8. Cingolani G, Petosa C, Weis K, Muller CW. 1999. Structure of importin-beta bound to the IBB domain of importinalpha. Nature 399:221-229. doi: 10.1038/20367.
9. Conti E, Uy M, Leighton L, Blobel G, Kuriyan J. 1998. Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell 94:193-204. doi: 10.1016/S0092-8674(00)81419-1.
10. Dong X, Biswas A, Suel KE, Jackson LK, Martinez R, Gu H, Chook YM. 2009. Structural basis for leucine-rich nuclear export signal recognition by CRM1. Nature 458:1136-1141. doi: 10.1038/nature07975.
11. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallographica. Section D, Biological Crystallography 66:486-501. doi: 10.1107/S0907444910007493.
12. Etchin J, Sun Q, Kentsis A, Farmer A, Zhang ZC, Sanda T, Mansour MR, Barcelo C, McCauley D, Kauffman M, Shacham S, Christie AL, Kung AL, Rodig SJ, Chook YM, Look AT. 2013. Antileukemic activity of nuclear export inhibitors that spare normal hematopoietic cells. Leukemia 27:66-74. doi: 10.1038/leu.2012.219.
13. Feng S, Chen JK, Yu H, Simon JA, Schreiber SL. 1994. Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science 266:1241-1247. doi: 10.1126/science.7526465.
14. Fontes MR, Teh T, Kobe B. 2000. Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-alpha. Journal of Molecular Biology 297:1183-1194. doi: 10.1006/jmbi.2000.3642.
15. Fornerod M, Ohno M, Yoshida M, Mattaj IW. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90:1051-1060. doi: 10.1016/S0092-8674(00)80371-2.
16. Fu SC, Huang HC, Horton P, Juan HF. 2013. ValidNESs: a database of validated leucine-rich nuclear export signals. Nucleic Acids Research 41:338-343. doi: 10.1093/nar/gks936.
17. Fu SC, Imai K, Horton P. 2011. Prediction of leucine-rich nuclear export signal containing proteins with NESsential. Nucleic Acids Research 39:e111. doi: 10.1093/nar/gkr493.
18. Fukuda M, Asano S, Nakamura T, Adachi M, Yoshida M, Yanagida M, Nishida E. 1997. CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 390:308-311. doi: 10.1038/36894.
19. Fung HY, Chook YM. 2014. Atomic basis of CRM1-cargo recognition, release and inhibition. Seminars in Cancer Biology 27:52-61. doi: 10.1016/j.semcancer.2014.03.002.
20. Guttler T, Madl T, Neumann P, Deichsel D, Corsini L, Monecke T, Ficner R, Sattler M, Gorlich D. 2010. NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nature Structural & Molecular Biology 17:1367-1376. doi: 10.1038/nsmb.1931.
21. Haines JD, Herbin O, de la Hera B, Vidaurre OG, Moy GA, Sun Q, Fung HY, Albrecht S, Alexandropoulos K, McCauley D, Chook YM, Kuhlmann T, Kidd GJ, Shacham S, Casaccia P. 2015. Nuclear export inhibitors avert progression in preclinical models of inflammatory demyelination. Nature neuroscience 18:511-520. doi: 10.1038/nn.3953.
22. Janda CY, Li J, Oubridge C, Hernandez H, Robinson CV, Nagai K. 2010. Recognition of a signal peptide by the signal recognition particle. Nature 465:507-510. doi: 10.1038/nature08870.
23. Kobayashi J, Hirano H, Matsuura Y. 2015. Crystal structure of the karyopherin Kap121p bound to the extreme C-terminus of the protein phosphatase Cdc14p. Biochemical and Biophysical Research Communications 463:309-314. doi: 10.1016/j.bbrc.2015.05.060.
24. Kosugi S, Hasebe M, Tomita M, Yanagawa H. 2008. Nuclear export signal consensus sequences defined using a localization-based yeast selection system. Traffic 9:2053-2062. doi: 10.1111/j.1600-0854.2008.00825.x.
25. Koyama M, Matsuura Y. 2010. An allosteric mechanism to displace nuclear export cargo from CRM1 and RanGTP by RanBP1. The EMBO Journal 29:2002-2013. doi: 10.1038/emboj.2010.89.
26. Koyama M, Shirai N, Matsuura Y. 2014. Structural insights into how Yrb2p accelerates the assembly of the Xpo1p nuclear export complex. Cell Reports 9:983-995. doi: 10.1016/j.celrep.2014.09.052.
27. Kutay U, Guttinger S. 2005. Leucine-rich nuclear-export signals: born to be weak. Trends in Cell Biology 15:121-124. doi: 10.1016/j.tcb.2005.01.005.
28. la Cour T, Kiemer L, Molgaard A, Gupta R, Skriver K, Brunak S. 2004. Analysis and prediction of leucine-rich nuclear export signals. Protein Engineering, Design & Selection 17:527-536. doi: 10.1093/protein/gzh062.
29. Lapalombella R, Sun Q, Williams K, Tangeman L, Jha S, Zhong Y, Goettl V, Mahoney E, Berglund C, Gupta S, Farmer A, Mani R, Johnson AJ, Lucas D, Mo X, Daelemans D, Sandanayaka V, Shechter S, McCauley D, Shacham S, Kauffman M, Chook YM, Byrd JC. 2012. Selective inhibitors of nuclear export show that CRM1/XPO1 is a target in chronic lymphocytic leukemia. Blood 120:4621-4634. doi: 10.1182/blood-2012-05-429506.
30. Lee BJ, Cansizoglu AE, Suel KE, Louis TH, Zhang Z, Chook YM. 2006. Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell 126:543-558. doi: 10.1016/j.cell.2006.05.049.
31. Lim WA, Richards FM, Fox RO. 1994. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature 372:375-379. doi: 10.1038/372375a0.
32. Lorenz S, Vakonakis I, Lowe ED, Campbell ID, Noble ME, Hoellerer MK. 2008. Structural analysis of the interactions between paxillin LD motifs and alpha-parvin. Structure 16:1521-1531. doi: 10.1016/j.str.2008.08.007.
33. Minor W, Cymborowski M, Otwinowski Z, Chruszcz M. 2006. HKL-3000: the integration of data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallographica. Section D, Biological Crystallography 62:859-866. doi: 10.1107/S0907444906019949.
34. Monecke T, Guttler T, Neumann P, Dickmanns A, Gorlich D, Ficner R. 2009. Crystal structure of the nuclear export receptor CRM1 in complex with Snurportin1 and RanGTP. Science 324:1087-1091. doi: 10.1126/science.1173388.
35. Neufeld C, Filipp FV, Simon B, Neuhaus A, Schuller N, David C, Kooshapur H, Madl T, Erdmann R, Schliebs W, Wilmanns M, Sattler M. 2009. Structural basis for competitive interactions of Pex14 with the import receptors Pex5 and Pex19. The EMBO Journal 28:745-754. doi: 10.1038/emboj.2009.7.
36. Ng C, Jackson RA, Buschdorf JP, Sun Q, Guy GR, Sivaraman J. 2008. Structural basis for a novel intrapeptidyl H-bond and reverse binding of c-Cbl-TKB domain substrates. The EMBO Journal 27:804-816. doi: 10.1038/emboj.2008.18.
37. Osawa M, Tokumitsu H, Swindells MB, Kurihara H, Orita M, Shibanuma T, Furuya T, Ikura M. 1999. A novel target recognition revealed by calmodulin in complex with Ca2+-calmodulin-dependent kinase kinase. Nature structural biology 6:819-824. doi: 10.1038/12271.
38. Ossareh-Nazari B, Bachelerie F, Dargemont C. 1997. Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science 278:141-144. doi: 10.1126/science.278.5335.141.
39. Praznikar J, Afonine PV, Guncar G, Adams PD, Turk D. 2009. Averaged kick maps: less noise, more signal and probably less bias. Acta Crystallographica. Section D, Biological Crystallography 65:921-931. doi: 10.1107/S0907444909021933.
40. Schrodinger LLC. 2010. The PyMOL molecular graphics system, version 1.7.0.1.
41. Song J, Zhang Z, Hu W, Chen Y. 2005. Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. The Journal of Biological Chemistry 280:40122-40129. doi: 10.1074/jbc.M507059200.
42. Soniat M, Chook YM. 2015. Nuclear localization signals for four distinct karyopherin-beta nuclear import systems. The Biochemical Journal 468:353-362. doi: 10.1042/BJ20150368.
43. Soniat M, Sampathkumar P, Collett G, Gizzi AS, Banu RN, Bhosle RC, Chamala S, Chowdhury S, Fiser A, Glenn AS, Hammonds J, Hillerich B, Khafizov K, Love JD, Matikainen B, Seidel RD, Toro R, Rajesh Kumar P, Bonanno JB, Chook YM, Almo SC. 2013. Crystal structure of human Karyopherin beta2 bound to the PY-NLS of Saccharomyces cerevisiae Nab2. Journal of Structural and Functional Genomics 14:31-35. doi: 10.1007/s10969-013-9150-1.
44. Sun Q, Carrasco YP, Hu Y, Guo X, Mirzaei H, Macmillan J, Chook YM. 2013. Nuclear export inhibition through covalent conjugation and hydrolysis of Leptomycin B by CRM1. Proceedings of the National Academy of Sciences of USA 110:1303-1308. doi: 10.1073/pnas.1217203110.
45. Swanson KA, Knoepfler PS, Huang K, Kang RS, Cowley SM, Laherty CD, Eisenman RN, Radhakrishnan I. 2004. HBP1 and Mad1 repressors bind the Sin3 corepressor PAH2 domain with opposite helical orientations. Nature Structural & Molecular Biology 11:738-746. doi: 10.1038/nsmb798.
46. Xu D, Farmer A, Chook YM. 2010. Recognition of nuclear targeting signals by Karyopherin-beta proteins. Current Opinion in Structural Biology 20:782-790. doi: 10.1016/j.sbi.2010.09.008.
47. Xu D, Farmer A, Collett G, Grishin NV, Chook YM. 2012a. Sequence and structural analyses of nuclear export signals in the NESdb database. Molecular Biology of the Cell 23:3677-3693. doi: 10.1091/mbc.E12-01-0046.
48. Xu D, Grishin NV, Chook YM. 2012b. NESdb: a database of NES-containing CRM1 cargoes. Molecular Biology of the Cell 23:3673-3676. doi: 10.1091/mbc.E12-01-0045.
49. Xu D, Marquis K, Pei J, Fu SC, Cagatay T, Grishin NV, Chook YM. 2015. LocNES: a computational tool for locating classical NESs in CRM1 cargo proteins. Bioinformatics 31:1357-1365. doi: 10.1093/bioinformatics/btu826.