Analysis of influenza A virus NS1 dimer interfaces in solution by pulse EPR distance measurements

Journal of Physical Chemistry B

Volumn 118, Issue 37, 2014, Pages 10882-10888

  Kerry, Philip S ^a   Turkington, Hannah L ^a,c   Ackermann, Katrin ^a,b   Jameison, Stephen A ^a   Bode, Bela E ^a,b  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c MRC CVR ^*  (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER INTERFACE; INFLUENZA A VIRUS; PULSE EPR;

INS1 PROTEIN, INFLUENZA VIRUS; SOLUTION AND SOLUBILITY; SPIN LABELING; VIRUS PROTEIN;

CHEMISTRY; ELECTRON SPIN RESONANCE; INFLUENZA VIRUS A; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SOLUTION AND SOLUBILITY; SPIN LABELING;

ELECTRON SPIN RESONANCE SPECTROSCOPY; INFLUENZA A VIRUS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SOLUTIONS; SPIN LABELS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84907720780     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp508386r     Document Type: Article

References (41)

1. Influenza Fact Sheet No. 211; World Health Organization: 2009.
2. Hale, B. G.; Randall, R. E.; Ortin, J.; Jackson, D. The Multifunctional NS1 Protein of Influenza A Viruses J. Gen. Virol. 2008, 89, 2359-2376
3. Kochs, G.; Garcia-Sastre, A.; Martinez-Sobrido, L. Multiple Anti-Interferon Actions of the Influenza A Virus NS1 Protein J. Virol. 2007, 81, 7011-7021
4. Guo, Z.; Chen, L. M.; Zeng, H.; Gomez, J. A.; Plowden, J.; Fujita, T.; Katz, J. M.; Donis, R. O.; Sambhara, S. NS1 Protein of Influenza A Virus Inhibits the Function of Intracytoplasmic Pathogen Sensor, RIG-I Am. J. Respir. Cell Mol. Biol. 2007, 36, 263-269
5. Gack, M. U.; Albrecht, R. A.; Urano, T.; Inn, K. S.; Huang, I. C.; Carnero, E.; Farzan, M.; Inoue, S.; Jung, J. U.; Garcia-Sastre, A. Influenza A Virus NS1 Targets the Ubiquitin Ligase TRIM25 to Evade Recognition by the Host Viral RNA Sensor RIG-I Cell Host Microbe 2009, 5, 439-449
6. Nemeroff, M. E.; Barabino, S. M.; Li, Y.; Keller, W.; Krug, R. M. Influenza Virus NS1 Protein Interacts with the Cellular 30 kDa Subunit of CPSF and Inhibits 3' End Formation of Cellular Pre-mRNAs Mol. Cell 1998, 1, 991-1000
7. Qian, X. Y.; Chien, C. Y.; Lu, Y.; Montelione, G. T.; Krug, R. M. An Amino- Terminal Polypeptide Fragment of the Influenza Virus NS1 Protein Possesses Specific RNA Binding Activity and Largely Helical Backbone Structure RNA 1995, 1, 948-956
8. Hale, B. G.; Jackson, D.; Chen, Y. H.; Lamb, R. A.; Randall, R. E. Influenza A Virus NS1 Protein Binds p85beta and Activates Phosphatidylinositol-3-Kinase Signaling Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 14194-14199
9. Burgui, I.; Aragon, T.; Ortin, J.; Nieto, A. PABP1 and eIF4GI Associate with Influenza Virus NS1 Protein in Viral mRNA Translation Initiation Complexes J. Gen. Virol. 2003, 84, 3263-3274
10. Bornholdt, Z. A.; Prasad, B. V. X-Ray Structure of Influenza Virus NS1 Effector Domain Nat. Struct. Mol. Biol. 2006, 13, 559-560
11. Bornholdt, Z. A.; Prasad, B. V. X-Ray Structure of NS1 from a Highly Pathogenic H5N1 Influenza Virus Nature 2008, 456, 985-988
12. Chien, C. Y.; Tejero, R.; Huang, Y.; Zimmerman, D. E.; Rios, C. B.; Krug, R. M.; Montelione, G. T. A Novel RNA-Binding Motif in Influenza A Virus Non-Structural Protein 1 Nat. Struct. Biol. 1997, 4, 891-895
13. Hale, B. G.; Barclay, W. S.; Randall, R. E.; Russell, R. J. Structure of an Avian Influenza A Virus NS1 Protein Effector Domain Virology 2008, 378, 1-5
14. Liu, J.; Lynch, P. A.; Chien, C. Y.; Montelione, G. T.; Krug, R. M.; Berman, H. M. Crystal Structure of the Unique RNA-Binding Domain of the Influenza Virus NS1 Protein Nat. Struct. Biol. 1997, 4, 896-899
15. Nemeroff, M. E.; Qian, X. Y.; Krug, R. M. The Influenza Virus NS1 Protein Forms Multimers in Vitro and in Vivo Virology 1995, 212, 422-428
16. Carrillo, B.; Choi, J. M.; Bornholdt, Z. A.; Sankaran, B.; Rice, A. P.; Prasad, B. V. The Influenza A Virus Protein NS1 Displays Structural Polymorphism J. Virol. 2014, 88, 4113-4122
17. Fremont, D. H.; Yu, Y. Y. L.; Nelson, C. A. Center for Structural Genomics of Infections Diseases (CSGID). Crystal Structure of Swine Flu Virus NS1 Effector Domain from H1N1 Influenza A/California/07/ 2009.
18. Kerry, P. S.; Ayllon, J.; Taylor, M. A.; Hass, C.; Lewis, A.; Garcia-Sastre, A.; Randall, R. E.; Hale, B. G.; Russell, R. J. A Transient Homotypic Interaction Model for the Influenza A Virus NS1 Protein Effector Domain PLoS One 2011, 6, e17946
19. Xia, S.; Monzingo, A. F.; Robertus, J. D. Structure of NS1A Effector Domain from the Influenza A/Udorn/72 Virus Acta Crystallogr., Sect. D: Biol. Crystallogr. 2009, 65, 11-17
20. Bornholdt, A.; Carrillo, B.; Prasad, B. V. V. In Influenza: Molecular Virology; Wang, Q.; Tao, Y. J., Eds.; Caister Academic Press: Norfolk, U.K., 2010; p 15-28.
21. 19F NMR Reveals Multiple Conformations at the Dimer Interface of the Nonstructural Protein 1 Effector Domain from Influenza A Virus Structure 2014, 22, 515-525
22. Aramini, J. M.; Ma, L. C.; Zhou, L.; Schauder, C. M.; Hamilton, K.; Amer, B. R.; Mack, T. R.; Lee, H. W.; Ciccosanti, C. T.; Zhao, L.; Xiao, R.; Krug, R. M.; Montelione, G. T. Dimer Interface of the Effector Domain of Non-structural Protein 1 from Influenza A Virus: an Interface with Multiple Functions J. Biol. Chem. 2011, 286, 26050-26060
23. Kerry, P. S.; Long, E.; Taylor, M. A.; Russell, R. J. Conservation of a Crystallographic Interface Suggests a Role for Beta-Sheet Augmentation in Influenza Virus NS1 Multifunctionality Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 2011, 67, 858-861
24. Xia, S.; Robertus, J. D. X-Ray Structures of NS1 Effector Domain Mutants Arch. Biochem. Biophys. 2010, 494, 198-204
25. Ayllon, J.; Russell, R. J.; Garcia-Sastre, A.; Hale, B. G. Contribution of NS1 Effector Domain Dimerization to Influenza A Virus Replication and Virulence J. Virol. 2012, 86, 13095-13098
26. Milov, A. D.; Salikov, K. M.; Shirov, M. D. Application of ELDOR in Electron-Spin Echo for Paramagnetic Center Space Distribution in Solids Fiz. Tverd. Tela 1981, 23, 975
27. Altenbach, C.; Flitsch, S. L.; Khorana, H. G.; Hubbell, W. L. Structural Studies on Transmembrane Proteins. 2. Spin Labeling of Bacteriorhodopsin Mutants at Unique Cysteines Biochemistry 1989, 28, 7806-7812
28. Pannier, M.; Veit, S.; Godt, A.; Jeschke, G.; Spiess, H. W. Dead-Time Free Measurement of Dipole-Dipole Interactions between Spins J. Magn. Reson. 2000, 142, 331-340
29. Jeschke, G. DEER Distance Measurements on Proteins Annu. Rev. Phys. Chem. 2012, 63, 419-446
30. Schiemann, O.; Weber, A.; Edwards, T. E.; Prisner, T. F.; Sigurdsson, S. T. Nanometer Distance Measurements on RNA Using PELDOR J. Am. Chem. Soc. 2003, 125, 3434-3435
31. Pliotas, C.; Ward, R.; Branigan, E.; Rasmussen, A.; Hagelueken, G.; Huang, H.; Black, S. S.; Booth, I. R.; Schiemann, O.; Naismith, J. H. Conformational State of the MscS Mechanosensitive Channel in Solution Revealed by Pulsed Electron-Electron Double Resonance (PELDOR) Spectroscopy Proc. Natl. Acad. Sci. U.S.A. 2012, 109, E2675
32. Hagelueken, G.; Ward, R.; Naismith, J.; Schiemann, O. MtsslWizard: In Silico Spin-Labeling and Generation of Distance Distributions in PyMOL Appl. Magn. Reson. 2012, 42, 377-391
33. Polyhach, Y.; Jeschke, G. Prediction of Favourable Sites for Spin Labelling of Proteins Spectroscopy 2010, 24, 651-659
34. Krivov, G. G.; Shapovalov, M. V.; Dunbrack, R. L., Jr. Improved Prediction of Protein Side-Chain Conformations with SCWRL4 Proteins 2009, 77, 778-795
35. Bode, B. E.; Margraf, D.; Plackmeyer, J.; Dürner, G.; Prisner, T. F.; Schiemann, O. Counting the Monomers in Nanometer-Sized Oligomers by Pulsed Electron-Electron Double Resonance J. Am. Chem. Soc. 2007, 129, 6736-6745
36. Jeschke, G.; Chechik, V.; Ionita, P.; Godt, A.; Zimmermann, H.; Banham, J.; Timmel, C. R.; Hilger, D.; Jung, H. DeerAnalysis2006 a Comprehensive Software Package for Analyzing Pulsed ELDOR Data Appl. Magn. Reson. 2006, 30, 473-498
37. Chiang, Y.-W.; Borbat, P. P.; Freed, J. H. The Determination of Pair Distance Distributions by Pulsed ESR using Tikhonov Regularization J. Magn. Reson. 2005, 172, 279-295
38. Giannoulis, A.; Ward, R.; Branigan, E.; Naismith, J. H.; Bode, B. E. PELDOR in Rotationally Symmetric Homo-Oligomers Mol. Phys. 2013, 111, 2845-2854
39. Jeschke, G. Conformational Dynamics and Distribution of Nitroxide Spin Labels Prog. Nucl. Magn. Reson. Spectrosc. 2013, 72, 42-60
40. Florin, N.; Schiemann, O.; Hagelueken, G. High-Resolution Crystal Structure of Spin Labelled (T21R1) Azurin from Pseudomonas Aeruginosa: a Challenging Structural Benchmark for In Silico Spin Labelling Algorithms BMC Struct. Biol. 2014, 14, 16
41. Das, K.; Ma, L. C.; Xiao, R.; Radvansky, B.; Aramini, J.; Zhao, L.; Marklund, J.; Kuo, R. L.; Twu, K. Y.; Arnold, E.; Krug, R. M.; Montelione, G. T. Structural Basis for Suppression of a Host Antiviral Response by Influenza A Virus Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 13093-13098