Ebola virus VP24 targets a unique NLS binding site on karyopherin alpha 5 to selectively compete with nuclear import of phosphorylated STAT1

Cell Host and Microbe

Volumn 16, Issue 2, 2014, Pages 187-200

  Xu, Wei ^a   Edwards, Megan R ^b   Borek, Dominika M ^c   Feagins, Alicia R ^b   Mittal, Anuradha ^d   Alinger, Joshua B ^a   Berry, Kayla N ^a   Yen, Benjamin ^b   Hamilton, Jennifer ^b   Brett, Tom J ^a   Pappu, Rohit V ^d   Leung, Daisy W ^a   Basler, Christopher F ^b   Amarasinghe, Gaya K ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

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

^d WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; KARYOPHERIN ALPHA; KARYOPHERIN ALPHA 5; PROTEIN VP24; STAT1 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; KARYOPHERIN ALPHA 5, HUMAN; NUCLEAR LOCALIZATION SIGNAL; PHOSPHOPROTEIN; STAT1 PROTEIN, HUMAN; VIRAL PROTEIN; VP24 PROTEIN, EBOLA VIRUS;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EBOLA VIRUS; EMBRYO; HUMAN; HUMAN CELL; INNATE IMMUNITY; MUTATION; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; VIRUS REPLICATION; ACTIVE TRANSPORT; BINDING COMPETITION; CELL NUCLEUS; CHEMICAL STRUCTURE; CHEMISTRY; EBOLAVIRUS; HEK293 CELL LINE; HYDROGEN BOND; METABOLISM; PHYSIOLOGY; PROTEIN DOMAIN; X RAY CRYSTALLOGRAPHY;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; BINDING, COMPETITIVE; CELL NUCLEUS; CRYSTALLOGRAPHY, X-RAY; EBOLAVIRUS; HEK293 CELLS; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; NUCLEAR LOCALIZATION SIGNALS; PHOSPHOPROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; STAT1 TRANSCRIPTION FACTOR; VIRAL PROTEINS;

EID: 84908332680     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.07.008     Document Type: Article

References (44)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. C.F. Basler, and G.K. Amarasinghe Evasion of interferon responses by Ebola and Marburg viruses J. Interferon Cytokine Res. 29 2009 511 520
3. M. Bray, and F.A. Murphy Filovirus research: knowledge expands to meet a growing threat J. Infect. Dis. 196 Suppl 2 2007 S438 S443
4. X. Chen, U. Vinkemeier, Y. Zhao, D. Jeruzalmi, J.E. Darnell Jr., and J. Kuriyan Crystal structure of a tyrosine phosphorylated STAT-1 dimer bound to DNA Cell 93 1998 827 839
5. Y.M. Chook, and G. Blobel Karyopherins and nuclear import Curr. Opin. Struct. Biol. 11 2001 703 715
6. M.J. Ciancanelli, V.A. Volchkova, M.L. Shaw, V.E. Volchkov, and C.F. Basler Nipah virus sequesters inactive STAT1 in the nucleus via a P gene-encoded mechanism J. Virol. 83 2009 7828 7841
7. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
8. E. Conti, and E. Izaurralde Nucleocytoplasmic transport enters the atomic age Curr. Opin. Cell Biol. 13 2001 310 319
9. E. Conti, and J. Kuriyan Crystallographic analysis of the specific yet versatile recognition of distinct nuclear localization signals by karyopherin alpha Structure 8 2000 329 338
10. E. Conti, M. Uy, L. Leighton, G. Blobel, and J. Kuriyan Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha Cell 94 1998 193 204
11. A. Cook, F. Bono, M. Jinek, and E. Conti Structural biology of nucleocytoplasmic transport Annu. Rev. Biochem. 76 2007 647 671
12. I.W. Davis, A. Leaver-Fay, V.B. Chen, J.N. Block, G.J. Kapral, X. Wang, L.W. Murray, W.B. Arendall 3rd, J. Snoeyink, J.S. Richardson, and D.C. Richardson MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35 Web Server issue 2007 W375 W383
13. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA
14. M.R. Edwards, B. Johnson, C.E. Mire, W. Xu, R.S. Shabman, L.N. Speller, D.W. Leung, T.W. Geisbert, G.K. Amarasinghe, and C.F. Basler The Marburg virus VP24 protein interacts with Keap1 to activate the cytoprotective antioxidant response pathway Cell Rep 6 2014 1017 1025
15. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
16. H. Feldmann, and T.W. Geisbert Ebola haemorrhagic fever Lancet 377 2011 849 862
17. T.W. Geisbert, H.A. Young, P.B. Jahrling, K.J. Davis, T. Larsen, E. Kagan, and L.E. Hensley Pathogenesis of Ebola hemorrhagic fever in primate models: evidence that hemorrhage is not a direct effect of virus-induced cytolysis of endothelial cells Am. J. Pathol. 163 2003 2371 2382
18. S. Goodbourn, L. Didcock, and R.E. Randall Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures J. Gen. Virol. 81 2000 2341 2364
19. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637
20. R.L. Kaletsky, J.R. Francica, C. Agrawal-Gamse, and P. Bates Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein Proc. Natl. Acad. Sci. USA 106 2009 2886 2891
21. R.A. Laskowski Enhancing the functional annotation of PDB structures in PDBsum using key figures extracted from the literature Bioinformatics 23 2007 1824 1827
22. R.A. Laskowski, and M.B. Swindells LigPlot+: multiple ligand-protein interaction diagrams for drug discovery J. Chem. Inf. Model. 51 2011 2778 2786
23. D.W. Leung, K.C. Prins, C.F. Basler, and G.K. Amarasinghe Ebolavirus VP35 is a multifunctional virulence factor Virulence 1 2010 526 531
24. M. Mateo, S.P. Reid, L.W. Leung, C.F. Basler, and V.E. Volchkov Ebolavirus VP24 binding to karyopherins is required for inhibition of interferon signaling J. Virol. 84 2010 1169 1175
25. K.M. McBride, G. Banninger, C. McDonald, and N.C. Reich Regulated nuclear import of the STAT1 transcription factor by direct binding of importin-alpha EMBO J. 21 2002 1754 1763
26. K. Melen, R. Fagerlund, J. Franke, M. Kohler, L. Kinnunen, and I. Julkunen Importin alpha nuclear localization signal binding sites for STAT1, STAT2, and influenza A virus nucleoprotein J. Biol. Chem. 278 2003 28193 28200
27. T. Meyer, A. Begitt, I. Lödige, M. van Rossum, and U. Vinkemeier Constitutive and IFN-gamma-induced nuclear import of STAT1 proceed through independent pathways EMBO J. 21 2002 344 354
28. J. Nardozzi, N. Wenta, N. Yasuhara, U. Vinkemeier, and G. Cingolani Molecular basis for the recognition of phosphorylated STAT1 by importin alpha5 J. Mol. Biol. 402 2010 83 100
29. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
30. A. Pichlmair, K. Kandasamy, G. Alvisi, O. Mulhern, R. Sacco, M. Habjan, M. Binder, A. Stefanovic, C.A. Eberle, and A. Goncalves et al. Viral immune modulators perturb the human molecular network by common and unique strategies Nature 487 2012 486 490
31. N.C. Reich, and L. Liu Tracking STAT nuclear traffic Nat. Rev. Immunol. 6 2006 602 612
32. S.P. Reid, L.W. Leung, A.L. Hartman, O. Martinez, M.L. Shaw, C. Carbonnelle, V.E. Volchkov, S.T. Nichol, and C.F. Basler Ebola virus VP24 binds karyopherin alpha1 and blocks STAT1 nuclear accumulation J. Virol. 80 2006 5156 5167
33. S.P. Reid, C. Valmas, O. Martinez, F.M. Sanchez, and C.F. Basler Ebola virus VP24 proteins inhibit the interaction of NPI-1 subfamily karyopherin alpha proteins with activated STAT1 J. Virol. 81 2007 13469 13477
34. T. Sekimoto, N. Imamoto, K. Nakajima, T. Hirano, and Y. Yoneda Extracellular signal-dependent nuclear import of Stat1 is mediated by nuclear pore-targeting complex formation with NPI-1, but not Rch1 EMBO J. 16 1997 7067 7077
35. F. Tarendeau, J. Boudet, D. Guilligay, P.J. Mas, C.M. Bougault, S. Boulo, F. Baudin, R.W. Ruigrok, N. Daigle, and J. Ellenberg et al. Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit Nat. Struct. Mol. Biol. 14 2007 229 233
36. C. Valmas, M.N. Grosch, M. Schümann, J. Olejnik, O. Martinez, S.M. Best, V. Krähling, C.F. Basler, and E. Mühlberger Marburg virus evades interferon responses by a mechanism distinct from ebola virus PLoS Pathog. 6 2010 e1000721
37. U. Vinkemeier, S.L. Cohen, I. Moarefi, B.T. Chait, J. Kuriyan, and J.E. Darnell Jr. DNA binding of in vitro activated Stat1 alpha, Stat1 beta and truncated Stat1: interaction between NH2-terminal domains stabilizes binding of two dimers to tandem DNA sites EMBO J. 15 1996 5616 5626
38. A. Vitalis, and R.V. Pappu ABSINTH: a new continuum solvation model for simulations of polypeptides in aqueous solutions J. Comput. Chem. 30 2009 673 699
39. S. Wälde, K. Thakar, S. Hutten, C. Spillner, A. Nath, U. Rothbauer, S. Wiemann, and R.H. Kehlenbach The nucleoporin Nup358/RanBP2 promotes nuclear import in a cargo- and transport receptor-specific manner Traffic 13 2012 218 233
40. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, and A. McCoy et al. Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
41. M.L. Yarbrough, M.A. Mata, R. Sakthivel, and B.M. Fontoura Viral subversion of nucleocytoplasmic trafficking Traffic 15 2014 127 140
42. A.P. Zhang, D.M. Abelson, Z.A. Bornholdt, T. Liu, V.L. Woods Jr., and E.O. Saphire The ebolavirus VP24 interferon antagonist: know your enemy Virulence 3 2012 440 445
43. A.P. Zhang, Z.A. Bornholdt, T. Liu, D.M. Abelson, D.E. Lee, S. Li, V.L. Woods Jr., and E.O. Saphire The ebola virus interferon antagonist VP24 directly binds STAT1 and has a novel, pyramidal fold PLoS Pathog. 8 2012 e1002550
44. A.P. Zhang, Z.A. Bornholdt, D.M. Abelson, and E.O. Saphire Crystal structure of Marburg virus VP24 J. Virol. 88 2014 5859 5863