Ensemble structure of the modular and flexible full-length vesicular stomatitis virus phosphoprotein

Journal of Molecular Biology

Volumn 423, Issue 2, 2012, Pages 182-197

  Leyrat, Cédric ^a   Schneider, Robert ^b   Ribeiro Jr , Euripedes A ^a   Yabukarski, Filip ^a   Yao, Mingxi ^b   Gérard, Francine C A ^a   Jensen, Malene Ringkjobing ^b   Ruigrok, Rob W H ^a   Blackledge, Martin ^b   Jamin, Marc ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

intrinsically disordered regions; NMR; phosphoprotein; SAXS; vesicular stomatitis virus

Indexed keywords

UNCLASSIFIED DRUG; VESICULAR STOMATITIS VIRUS PHOSPHOPROTEIN; VIRUS PHOSPHOPROTEIN;

ARTICLE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; VESICULAR STOMATITIS VIRUS; VIRUS REPLICATION; VIRUS TRANSCRIPTION; X RAY CRYSTALLOGRAPHY;

RNA VIRUSES; VESICULAR STOMATITIS VIRUS;

EID: 84866501486     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.07.003     Document Type: Article

References (102)

1. R.A. Lamb Mononegavirales D.M. Knipe, P.M. Howley, 5th Ed Fields Virology 1 2007 Lippincott Williams & Wilkins Philadelphia, PA 1357 1361
2. D.S. Lyles, and C.E. Rupprecht Rhabdoviridae D.M. Knipe, P.M. Howley, 5th Ed Fields Virology 1 2007 Lippincott Williams & Wilkins Philadelphia, PA 1363 1408
3. T.J. Green, X. Zhang, G.W. Wertz, and M. Luo Structure of the vesicular stomatitis virus nucleoprotein-RNA complex Science 313 2006 357 360
4. H. Arnheiter, N.L. Davis, G. Wertz, M. Schubert, and R.A. Lazzarini Role of the nucleocapsid protein in regulating vesicular stomatitis virus RNA synthesis Cell 41 1985 259 267
5. S.U. Emerson, and Y. Yu Both NS and L proteins are required for in vitro RNA synthesis by vesicular stomatitis virus J. Virol. 15 1975 1348 1356
6. S.P. Whelan, J.N. Barr, and G.W. Wertz Transcription and replication of nonsegmented negative-strand RNA viruses Curr. Top. Microbiol. Immunol. 283 2004 61 119
7. J. Li, J.T. Wang, and S.P. Whelan A unique strategy for mRNA cap methylation used by vesicular stomatitis virus Proc. Natl Acad. Sci. USA 103 2006 8493 8498
8. S.A. Moyer, and A.K. Banerjee Messenger RNA species synthesized in vitro by the virion-associated RNA polymerase of vesicular stomatitis virus Cell 4 1975 37 43
9. G. Abraham, D.P. Rhodes, and A.K. Banerjee The 5′ terminal structure of the methylated mRNA synthesized in vitro by vesicular stomatitis virus Cell 5 1975 51 58
10. N. Hercyk, S.M. Horikami, and S.A. Moyer The vesicular stomatitis virus L protein possesses the mRNA methyltransferase activities Virology 163 1988 222 225
11. J.N. Barr, and G.W. Wertz Polymerase slippage at vesicular stomatitis virus gene junctions to generate poly(A) is regulated by the upstream 3′-AUAC-5′ tetranucleotide: implications for the mechanism of transcription termination J. Virol. 75 2001 6901 6913
12. M.G. Mellon, and S.U. Emerson Rebinding of transcriptase components (L and NS proteins) to the nucleocapsid template of vesicular stomatitis virus J. Virol. 27 1978 560 567
13. B. Morin, A.A. Rahmeh, and S.P. Whelan Mechanism of RNA synthesis initiation by the vesicular stomatitis virus polymerase EMBO J. 31 2012 1320 1329
14. S.U. Emerson, and M. Schubert Location of the binding domains for the RNA polymerase L and the ribonucleocapsid template within different halves of the NS phosphoprotein of vesicular stomatitis virus Proc. Natl Acad. Sci. U.S.A. 84 1987 5655 5659
15. R.W. Peluso, and S.A. Moyer Viral proteins required for the in vitro replication of vesicular stomatitis virus defective interfering particle genome RNA Virology 162 1988 369 376
16. 0-P complex PLoS Pathogens 7 2011 e1002248
17. 0-P complex formation and encapsidation of viral genome RNA J. Virol. 81 2007 13478 13485
18. P.S. Masters, and A.K. Banerjee Complex formation with vesicular stomatitis virus phosphoprotein NS prevents binding of nucleocapsid protein N to nonspecific RNA J. Virol. 62 1988 2658 2664
19. F.C.A. Gérard, A. Ribeiro Ede Jr, A.A. Albertini, I. Gutsche, G. Zaccai, R.W. Ruigrok, and M. Jamin Unphosphorylated Rhabdoviridae phosphoproteins form elongated dimers in solution Biochemistry 46 2007 10328 10338
20. S.C. Das, and A.K. Pattnaik Role of the hypervariable hinge region of phosphoprotein P of vesicular stomatitis virus in viral RNA synthesis and assembly of infectious virus particles J. Virol. 79 2005 8101 8112
21. T. Das, A.K. Pattnaik, A.M. Takacs, T. Li, L.N. Hwang, and A.K. Banerjee Basic amino acid residues at the carboxy-terminal eleven amino acid region of the phosphoprotein (P) are required for transcription but not for replication of vesicular stomatitis virus genome RNA Virology 238 1997 103 114
22. A.M. Takacs, T. Das, and A.K. Banerjee Mapping of interacting domains between the nucleocapsid protein and the phosphoprotein of vesicular stomatitis virus by using a two-hybrid system Proc. Natl Acad. Sci. U.S.A. 90 1993 10375 10379
23. H. Ding, T.J. Green, S. Lu, and M. Luo Crystal structure of the oligomerization domain of the phosphoprotein of vesicular stomatitis virus J. Virol. 80 2006 2808 2814
24. H. Ding, T.J. Green, and M. Luo Crystallization and preliminary X-ray analysis of a proteinase-K-resistant domain within the phosphoprotein of vesicular stomatitis virus (Indiana) Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2087 2090
25. F.C.A. Gérard, A. Ribeiro Ede Jr, C. Leyrat, I. Ivanov, D. Blondel, and S. Longhi Modular organization of rabies virus phosphoprotein J. Mol. Biol. 388 2009 978 996
26. E.A. Ribeiro Jr, A. Favier, F.C. Gerard, C. Leyrat, B. Brutscher, and D. Blondel Solution structure of the C-terminal nucleoprotein-RNA binding domain of the vesicular stomatitis virus phosphoprotein J. Mol. Biol. 382 2008 525 538
27. T.J. Green, S. Macpherson, S. Qiu, J. Lebowitz, G.W. Wertz, and M. Luo Study of the assembly of vesicular stomatitis virus N protein: role of the P protein J. Virol. 74 2000 9515 9524
28. 0-binding region of the vesicular stomatitis virus phosphoprotein is globally disordered but contains transient α-helices Protein Sci. 20 2011 542 556
29. C. Leyrat, F.C. Gérard, E. de Almeida Ribeiro Jr, I. Ivanov, R.W. Ruigrok, and M. Jamin Structural disorder in proteins of the rhabdoviridae replication complex Protein Pept. Lett. 17 2010 979 987
30. C. Leyrat, E.A. Ribeiro, F.C.A. Gérard, I. Ivanov, R.W.H. Ruigrok, and M. Jamin Structure, interactions with host cell and functions of rhabdovirus phosphoprotein Future Virol. 6 2011 465 481
31. H.J. Dyson, and P.E. Wright Intrinsically unstructured proteins and their functions Nat. Rev., Mol. Cell Biol. 6 2005 197 208
32. A.K. Dunker, Z. Obradovic, P. Romero, E.C. Garner, and C.J. Brown Intrinsic protein disorder in complete genomes Genome Inf. Ser. Workshop Genome Inf. 11 2000 161 171
33. P. Bernado Effect of interdomain dynamics on the structure determination of modular proteins by small-angle scattering Eur. J. Biophys. 39 2010 769 780
34. P. Bernado, and M. Blackledge Structural biology: proteins in dynamic equilibrium Nature 468 2010 1046 1048
35. W.T. Heller Influence of multiple well defined conformations on small-angle scattering of proteins in solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 61 2005 33 44
36. R. Schneider, J. Huang, M. Yao, G. Communie, V. Ozenne, and L. Mollica Towards a robust description of intrinsic protein disorder using nuclear magnetic resonance spectroscopy Mol. BioSyst. 8 2012 58 68
37. H.J. Dyson, and P.E. Wright Unfolded proteins and protein folding studied by NMR Chem. Rev. 104 2004 3607 3622
38. P.B. Moore Small-angle scattering. Information content and error analysis J. Appl. Crystallogr. 13 1980 168 175
39. D.I. Svergun Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing Biophys. J. 76 1999 2879 2886
40. M.H. Koch, P. Vachette, and D.I. Svergun Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution Q. Rev. Biophys. 36 2003 147 227
41. H.D. Mertens, and D.I. Svergun Structural characterization of proteins and complexes using small-angle X-ray solution scattering J. Struct. Biol. 172 2010 128 141
42. C.D. Putnam, M. Hammel, G.L. Hura, and J.A. Tainer X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution Q. Rev. Biophys. 40 2007 191 285
43. J. Lipfert, and S. Doniach Small-angle X-ray scattering from RNA, proteins, and protein complexes Annu. Rev. Biophys. Biomol. Struct. 36 2007 307 327
44. R.P. Rambo, and J.A. Tainer Bridging the solution divide: comprehensive structural analyses of dynamic RNA, DNA, and protein assemblies by small-angle X-ray scattering Curr. Opin. Struct. Biol. 20 2010 128 137
45. G. Nodet, L. Salmon, V. Ozenne, S. Meier, M.R. Jensen, and M. Blackledge Quantitative description of backbone conformational sampling of unfolded proteins at amino acid resolution from NMR residual dipolar couplings J. Am. Chem. Soc. 131 2009 17908 17918
46. P. Bernado, L. Blanchard, P. Timmins, D. Marion, R.W.H. Ruigrok, and M. Blackledge A structural model for unfolded proteins from residual dipolar couplings and small-angle X-ray scattering Proc. Natl Acad. Sci. USA 102 2005 17002 17007
47. M.A. Jamros, L.C. Oliveira, P.C. Whitford, J.N. Onuchic, J.A. Adams, D.K. Blumenthal, and P.A. Jennings Proteins at work: a combined small angle X-ray scattering and theoretical determination of the multiple structures involved on the protein kinase functional landscape J. Biol. Chem. 285 2010 36121 36128
48. C.K. Fisher, A. Huang, and C.M. Stultz Modeling intrinsically disordered proteins with Bayesian statistics J. Am. Chem. Soc. 132 2010 14919 14927
49. M.R. Jensen, P.R. Markwick, S. Meier, C. Griesinger, M. Zweckstetter, and S. Grzesiek Quantitative determination of the conformational properties of partially folded and intrinsically disordered proteins using NMR dipolar couplings Structure 17 2009 1169 1185
50. M.R. Jensen, L. Salmon, G. Nodet, and M. Blackledge Defining conformational ensembles of intrinsically disordered and partially folded proteins directly from chemical shifts J. Am. Chem. Soc. 132 2010 1270 1272
51. D. Ganguly, and J. Chen Structural interpretation of paramagnetic relaxation enhancement-derived distances for disordered protein states J. Mol. Biol. 390 2009 467 477
52. M. Pelikan, G.L. Hura, and M. Hammel Structure and flexibility within proteins as identified through small angle X-ray scattering Gen. Physiol. Biophys. 28 2009 174 189
53. P. Bernado, E. Mylonas, M.V. Petoukhov, M. Blackledge, and D.I. Svergun Structural characterization of flexible proteins using small-angle X-ray scattering J. Am. Chem. Soc. 129 2007 5656 5664
54. M. Wells, H. Tidow, T.J. Rutherford, P. Markwick, M.R. Jensen, and E. Mylonas Structure of tumor suppressor p53 and its intrinsically disordered N-terminal transactivation domain Proc. Natl Acad. Sci. USA 105 2008 5762 5767
55. J.A. Marsh, and J.D. Forman-Kay Structure and disorder in an unfolded state under nondenaturing conditions from ensemble models consistent with a large number of experimental restraints J. Mol. Biol. 391 2009 359 374
56. M.R. Jensen, G. Communie, E.A. Ribeiro Jr, N. Martinez, A. Desfosses, and L. Salmon Intrinsic disorder in measles virus nucleocapsids Proc. Natl Acad. Sci. USA 108 2011 9839 9844
57. V.N. Uversky Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule Biochemistry 32 1993 13288 13298
58. O. Zhang, and J.D. Forman-Kay Structural characterization of folded and unfolded states of an SH3 domain in equilibrium in aqueous buffer Biochemistry 34 1995 6784 6794
59. D.S. Wishart, B.D. Sykes, and F.M. Richards Relationship between nuclear magnetic resonance chemical shift and protein secondary structure J. Mol. Biol. 222 1991 311 333
60. J.A. Marsh, V.K. Singh, Z. Jia, and J.D. Forman-Kay Sensitivity of secondary structure propensities to sequence differences between α- and γ-synuclein: implications for fibrillation Protein Sci. 15 2006 2795 2804
61. 13C nuclear magnetic resonance chemical shifts J. Am. Chem. Soc. 113 1991 5490 5492
62. S.H. Bae, H.J. Dyson, and P.E. Wright Prediction of the rotational tumbling time for proteins with disordered segments J. Am. Chem. Soc. 131 2009 6814 6821
63. G. Nicastro, P. Margiocco, B. Cardinali, P. Stagnaro, F. Cauglia, and C. Cuniberti The role of unstructured extensions in the rotational diffusion properties of a globular protein: the example of the titin i27 module Biophys. J. 87 2004 1227 1240
64. O. Glatter, and O. Kratky Small Angle X-ray Scattering 1982 Academic Press London, UK
65. P. Calmettes, D. Durand, M. Desmadril, P. Minard, V. Receveur, and J.C. Smith How random is a highly denatured protein? Biophys. Chem. 53 1994 105 113
66. M.V. Petoukhov, and D.I. Svergun Global rigid body modeling of macromolecular complexes against small-angle scattering data Biophys. J. 89 2005 1237 1250
67. P. Bernado, and D.I. Svergun Structural analysis of intrinsically disordered proteins by small-angle X-ray scattering Mol. BioSyst. 8 2012 151 167
68. V. Ozenne, F. Bauer, L. Salmon, J.R. Huang, M.R. Jensen, and S. Segard Flexible-meccano: a tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables Bioinformatics 28 2012 1463 1470
69. Y. Shen, and A. Bax Protein backbone chemical shifts predicted from searching a database for torsion angle and sequence homology J. Biomol. NMR 38 2007 289 302
70. D. Svergun, C. Barberato, and M.H. Koch CRYSOL - a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates J. Appl. Crystallogr. 28 1995 768 773
71. S. Muller-Späth, A. Soranno, V. Hirschfeld, H. Hofmann, S. Rüegger, and L. Reymond Charge interactions can dominate the dimensions of intrinsically disordered proteins Proc. Natl Acad. Sci. USA 107 2010 14609 14614
72. L. Salmon, G. Nodet, V. Ozenne, G. Yin, M.R. Jensen, M. Zweckstetter, and M. Blackledge NMR characterization of long-range order in intrinsically disordered proteins J. Am. Chem. Soc. 132 2010 8407 8418
73. M.R. Jensen, P. Bernadó, K. Houben, L. Blanchard, D. Marion, R.W. Ruigrok, and M. Blackledge Structural disorder within sendai virus nucleoprotein and phosphoprotein: insight into the structural basis of molecular recognition Protein Pept. Lett. 17 2010 952 960
74. J. Habchi, L. Mamelli, H. Darbon, and S. Longhi Structural disorder within Henipavirus nucleoprotein and phosphoprotein: from predictions to experimental assessment PLoS One 5 2010 e11684
75. J. Curran, R. Boeck, N. Lin-Marq, A. Lupas, and D. Kolakofsky Paramyxovirus phosphoproteins form homotrimers as determined by an epitope dilution assay, via predicted coiled coils Virology 214 1995 139 149
76. N. Tarbouriech, J. Curran, C. Ebel, R.W. Ruigrok, and W.P. Burmeister On the domain structure and the polymerization state of the sendai virus P protein Virology 266 2000 99 109
77. D. Karlin, F. Ferron, B. Canard, and S. Longhi Structural disorder and modular organization in Paramyxovirinae N and P J. Gen. Virol. 84 2003 3239 3252
78. M. Hock, I. Kraus, G. Schoehn, M. Jamin, C. Andrei-Selmer, W. Garten, and W. Weissenhorn RNA induced polymerization of the Borna disease virus nucleoprotein Virology 397 2009 64 72
79. B.A. Shoemaker, J.J. Portman, and P.G. Wolynes Speeding molecular recognition by using the folding funnel: the fly-casting mechanism Proc. Natl Acad. Sci. U.S.A. 97 2000 8868 8873
80. B.W. Pontius Close encounters: why unstructured, polymeric domains can increase rates of specific macromolecular association Trends Biochem. Sci. 18 1993 181 186
81. P. Ge, J. Tsao, S. Schein, T.J. Green, M. Luo, and Z.H. Zhou Cryo-EM model of the bullet-shaped vesicular stomatitis virus Science 327 2010 689 693
82. T.J. Green, and M. Luo Structure of the vesicular stomatitis virus nucleocapsid in complex with the nucleocapsid-binding domain of the small polymerase cofactor, P Proc. Natl Acad. Sci. USA 106 2009 11713 11718
83. D. Kolakofsky, P. Le Mercier, F. Iseni, and D. Garcin Viral RNA polymerase scanning and the gymnastics of Sendai virus RNA synthesis Virology 318 2004 463 473
84. J. Curran A role for the Sendai virus P protein trimer in RNA synthesis J. Virol. 72 1998 4274 4280
85. Y. Jacob, E. Real, and N. Tordo Functional interaction map of lyssavirus phosphoprotein: identification of the minimal transcription domains J. Virol. 75 2001 9613 9622
86. S.T. Milner Polymer brushes Science 251 1991 905 914
87. H.G. Brown, and J.H. Hoh Entropic exclusion by neurofilament sidearms: a mechanism for maintaining interfilament spacing Biochemistry 36 1997 15035 15040
88. R.Y. Lim, N.-P. Huang, J. Köser, J. Deng, K.H.A. Lau, and K. Schwarz-Herion Flexible phenylalanine-glycine nucleoporins as entropic barriers to nucleocytoplasmic transport Proc. Natl Acad. Sci. USA 103 2006 9512 9517
89. R. Mukhopadhyay, and J.H. Hoh AFM force measurements on microtubule-associated proteins: the projection domain exerts a long-range repulsive force FEBS Lett. 505 2001 374 378
90. D. Thomas, W.W. Newcomb, J.C. Brown, J.S. Wall, J.F. Hainfeld, B.L. Trus, and A.C. Steven Mass and molecular composition of vesicular stomatitis virus: a scanning transmission electron microscopy analysis J. Virol. 54 1985 598 607
91. H.J. Dyson, and P.E. Wright Coupling of folding and binding for unstructured proteins Curr. Opin. Struct. Biol. 12 2002 54 60
92. P.E. Wright, and H.J. Dyson Linking folding and binding Curr. Opin. Struct. Biol. 19 2009 31 38
93. A.K. Gupta, and A.K. Banerjee Expression and purification of vesicular stomatitis virus N-P complex from Escherichia coli: role in genome RNA transcription and replication in vitro J. Virol. 71 1997 4264 4271
94. A. Barge, Y. Gaudin, P. Coulon, and R.W. Ruigrok Vesicular stomatitis virus M protein may be inside the ribonucleocapsid coil J. Virol. 67 1993 7246 7253
95. P.J. Wyatt Submicrometer particle sizing by multiangle light scattering following fractionation J. Colloid Interface Sci. 197 1998 9 20
96. E. Lescop, P. Schanda, and B. Brutscher A set of BEST triple-resonance experiments for time-optimized protein resonance assignment J. Magn. Reson. 187 2007 163 169
97. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
98. T.D. Goddard, and D.G. Kneller SPARKY 3 2003 University of California San Francisco, CA
99. Y.S. Jung, and M. Zweckstetter Mars - robust automatic backbone assignment of proteins J. Biomol. NMR 30 2004 11 23
100. P.V. Konarev, V.V. Volkov, A. Sokolova, M.H.J. Koch, and D.I. Svergun PRIMUS: a Windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 36 2003 1277 1282
101. A.V. Semenyuk, and D. Svergun GNOM - a program package for small-angle scattering data processing J. Appl. Crystallogr. 24 1991 537 540
102. E. Eyal, R. Najmanovich, B.J. McConkey, M. Edelman, and V. Sobolev Importance of solvent accessibility and contact surfaces in modeling side-chain conformations in proteins J. Comput. Chem. 25 2004 712 724