Solution structure of the C-terminal X domain of the measles virus phosphoprotein and interaction with the intrinsically disordered C-terminal domain of the nucleoprotein

Journal of Molecular Recognition

Volumn 23, Issue 5, 2010, Pages 435-447

  Gely, Stéphane ^a   Lowry, David F ^b   Bernard, Cédric ^a   Jensen, Malene R ^c   Blackledge, Martin ^c   Costanzo, Stéphanie ^a   Bourhis, Jean Marie ^a,d   Darbon, Hervé ^a   Daughdrill, Gary ^b   Longhi, Sonia ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^d INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

Author keywords

Conformer selection; Disorder to order transitions; Induced folding; Intrinsic disorder; Measles virus; NMR spectral assignment; Nucleoprotein; Phosphoprotein; Residual structure; Solution structure

Indexed keywords

NUCLEOPROTEIN; PHOSPHOPROTEIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; MEASLES VIRUS; METABOLISM; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SOLUTION AND SOLUBILITY; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; MEASLES VIRUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEOPROTEINS; PHOSPHOPROTEINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SOLUTIONS;

MEASLES VIRUS;

EID: 77955378293     PISSN: 09523499     EISSN: 10991352     Source Type: Journal    
DOI: 10.1002/jmr.1010     Document Type: Article

References (56)

1. Albertini AA, Wernimont AK, Muziol T, Ravelli RB, Clapier CR, Schoehn G, WeissenhornW, Ruigrok RW. 2006. Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 313: 360-363.
2. Belle V, Rouger S, Costanzo S, Liquiere E, Strancar J, Guigliarelli B, Fournel A, Longhi S. 2008. Mapping alpha-helical induced folding within the intrinsically disordered C-terminal domain of the measles virus nucleoprotein by site-directed spin-labeling EPR spectroscopy. Proteins 73: 973-988.
3. Bernado P, Blanchard L, Timmins P, Marion D, Ruigrok RW, Blackledge M. 2005. A structural model for unfolded proteins from residual dipolar couplings and small-angle X-ray scattering. Proc. Natl Acad. Sci. USA 102: 17002-17007.
4. Bernard C, Gely S, Bourhis JM, Morelli X, Longhi S, Darbon H. 2009. Interaction between the C-terminal domains of N and P proteins of measles virus investigated by NMR. FEBS Lett. 583: 1084-1089.
5. Blanchard L, Tarbouriech N, Blackledge M, Timmins P, Burmeister WP, Ruigrok RW, Marion D. 2004. Structure and dynamics of the nucleocapsid- binding domain of the Sendai virus phosphoprotein in solution. Virology 319: 201-211.
6. Bourhis J, Johansson K, Receveur-Bréchot V, Oldfield CJ, Dunker AK, Canard B, Longhi S. 2004. The C-terminal domain of measles virus nucleoprotein belongs to the classof intrinsically disordered proteins that fold upon binding to their pohysiological partner. Virus Res. 99: 157-167.
7. Bourhis JM, Receveur-Bréchot V, Oglesbee M, Zhang X, Buccellato M, Darbon H, Canard B, Finet S, Longhi S. 2005a. The intrinsically disordered C-terminal domain of the measles virus nucleoprotein interacts with the C-terminal domain of the phosphoprotein via two distinct sites and remains predominantly unfolded. Protein Sci. 14: 1975-1992.
8. Bourhis JM, Canard B, Longhi S. 2005b. Désordre structural au sein du complexe réplicatif du virus de la rougeole: implications fonctionnelles. Virologie 9: 367-383.
9. Bourhis JM, Canard B, Longhi S. 2006. Structural disorder within the replicative complex of measles virus: functional implications. Virology 344: 94-110.
10. Bourhis JM, Longhi S. 2007. Measles virus nucleoprotein: structural organization and functional role of the intrinsically disordered C-terminal domain. In Measles Virus Nucleoprotein, Longhi S (ed.). Nova Publishers Inc.: Hauppage, NY; 1-35.
11. Curran JA, Kolakofsky D. 1991. Rescue of a Sendai virus DI genome by other parainfluenza viruses: implications for genome replication. Virology 182: 168-176.
12. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. 1995. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6: 277-293.
13. DeLano WL. 2002. The PyMOL molecular graphics system proteins: structure. Funct. Bioinform. 30: 442-454.
14. Farrow NA, Muhandiram R, Singer AU, Pascal SM, Kay CM, Gish G, Shoelson SE, Pawson T, Forman-Kay JD, Kay LE. 1994. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33: 5984-6003.
15. Fuxreiter M, Tompa P, Simon I. 2007. Local structural disorder imparts plasticity on linear motifs. Bioinformatics 23: 950-956.
16. Goddard TD, Kneller DG. 2003. University of California.
17. Green TJ, Zhang X, Wertz GW, Luo M. 2006. Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 313: 357-360.
18. Houben K, Marion D, Tarbouriech N, Ruigrok RW, Blanchard L. 2007a. Interaction of the C-terminal domains of sendai virus N and P proteins: comparison of polymerase-nucleocapsid interactions within the paramyxovirus family. J. Virol. 81: 6807-6816.
19. Houben K, Blanchard L, Blackledge M, Marion D. 2007b. Intrinsic dynamics of the partly unstructured PX domain from the Sendai virus RNA polymerase cofactor P. Biophys. J. 93: 2830-2844.
20. Jensen MR, Houben K, Lescop E, Blanchard L, Ruigrok RW, Blackledge M. 2008. Quantitative conformational analysis of partially folded proteins from residual dipolar couplings: application to the molecular recognition element of Sendai virus nucleoprotein. J. Am. Chem. Soc. 130: 8055-8061.
21. Johansson K, Bourhis JM, Campanacci V, Cambillau C, Canard B, Longhi S. 2003. Crystal structure of the measles virus phosphoprotein domain responsible for the induced folding of the C-terminal domain of the nucleoprotein. J. Biol. Chem. 278: 44567-44573.
22. Johnson BA, Blevins RA. 1994. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4: 603-614.
23. Jung YS, Zweckstetter M. 2004. Mars - robust automatic backbone assignment of proteins. J. Biomol. NMR 30: 11-23.
24. Karlin D, Ferron F, Canard B, Longhi S. 2003. Structural disorder and modular organization in Paramyxovirinae N and P. J. Gen. Virol. 84: 3239-3252.
25. Karlin D, Longhi S, Receveur V, Canard B. 2002a. The N-terminal domain of the phosphoprotein of morbilliviruses belongs to the natively unfolded class of proteins. Virology 296: 251-262.
26. Karlin D, Longhi S, Canard B. 2002b. Substitution of two residues in the measles virus nucleoprotein results in an impaired self-association. Virology 302: 420-432.
27. Kay LE, Keifer P, Saarinen T. 1992. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114: 10663.
28. Kingston RL, Gay LS, Baase WS, Matthews BW. 2008. Structure of the nucleocapsid-binding domain from the mumps virus polymerase; an example of protein folding induced by crystallization. J. Mol. Biol. 379: 719-71931.
29. Kingston RL, Hamel DJ, Gay LS, Dahlquist FW, Matthews BW. 2004a. Structural basis for the attachment of a paramyxoviral polymerase to its template. Proc. Natl Acad. Sci. USA 101: 8301-8306.
30. Kingston RL, Walter AB, Gay LS. 2004b. Characterization of nucleocapsid binding by the measles and the mumps virus phosphoprotein. J. Virol. 78: 8615-8629.
31. Laskowski RA, Mac Arthur MW, Moss DM, Thornton JM. 1993. A program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26: 283-291.
32. Lescop E, Schanda P, Brutscher B. 2007. A set of BEST triple-resonance experiments for time-optimized protein resonance assignment. J. Magn. Reson. 187: 163-169.
33. Linge JP, Habeck M, Rieping W, Nilges M. 2003. ARIA: Automated NOE assignment and NMR structure calculation. Bioinformatics 19: 315-316.
34. Longhi S, Canard B. 1999. Mécanismes de transcription et de réplacation des Paramyxoviridae. Virologie 3: 227-240.
35. Longhi S, Receveur-Brechot V, Karlin D, Johansson K, Darbon H, Bhella D, Yeo R, Finet S, Canard B. 2003. The C-terminal domain of the measles virus nucleoprotein is intrinsically disordered and folds upon binding to the C-terminal moiety of the phosphoprotein. J. Biol. Chem. 278: 18638-18648.
36. Longhi S. 2009. Nucleocapsid Structure and Function. Curr. Top. Microbiol. Immunol. 329: 103-128.
37. Macura S, Ernst RR. 1980. Elucidation of cross relaxation in liquids by two-dimensional N.M.R. spectroscopy. Mol. Phys. 41: 95-117.
38. Meszaros B, Tompa P, Simon I, Dosztanyi Z. 2007. Molecular principles of the interactions of disordered proteins. J. Mol. Biol. 372: 549-561.
39. Mohan A, Oldfield CJ, Radivojac P, Vacic V, Cortese MS, Dunker AK, Uversky VN. 2006. Analysis of Molecular Recognition Features (MoRFs). J. Mol. Biol. 362: 1043-1059.
40. Morin B, Bourhis JM, Belle V,Woudstra M, Carriere F, Bguigliarelli B, Fournel A, LonghiS., 2006. Assessing induced folding of an intrinsically disordered protein by site-directed spin-labeling EPR spectroscopy. J. Phys. Chem. B 110: 20596-20608.
41. Muhandiram DR, Kay LE. 1994. Gradient-enhanced triple-resonance threedimensional NMR Experiments with improved sensitivity. J. Magn. Reson. B 3: 203-216.
42. Mulder FA, Schipper D, Bott R, Boelens R. 1999. Altered flexibility in the substrate-binding site of related native and engineered high-alkaline Bacillus subtilisins. J. Mol. Biol. 292: 111-123.
43. Oldfield CJ, Cheng Y, Cortese MS, Romero P, Uversky VN, Dunker AK. 2005. Coupled folding and binding with alpha-helix-forming molecular recognition elements. Biochemistry 44: 12454-12470.
44. Schanda P, Van Melckebeke H, Brutscher B. 2006. Speeding up threedimensional protein NMR experiments to a few minutes. J. Am. Chem. Soc. 128: 9042-9043.
45. Schwarzinger S, Kroon GJ, Foss TR, Chung J, Wright PE, Dyson HJ. 2001. Sequence-dependent correction of random coil NMR chemical shifts. J. Am. Chem. Soc. 123: 2970-2978.
46. Schwarzinger S, Kroon GJ, Foss TR, Wright PE, Dyson HJ. 2000. Random coil chemical shifts in acidic 8M urea: implementation of random coil shift data in NMRView. J. Biomol. NMR 18: 43-48.
47. Sigalov AB, Zhuravleva AV, Orekhov VY. 2007. Binding of intrinsically disordered proteins is not necessarily accompanied by a structural transition to a folded form. Biochimie 89: 419-421.
48. Sigalov AB, Kim WM, Saline M, Stern LJ. 2008. The intrinsically disordered cytoplasmic domain of the T cell receptor zeta chain binds to the nef protein of simian immunodeficiency virus without a disorderto- order transition. Biochemistry 47: 12942-12944.
49. Tarbouriech N, Curran J, Ruigrok RW, Burmeister WP. 2000. Tetrameric coiled coil domain of Sendai virus phosphoprotein. Nat. Struct. Biol. 7: 777-781.
50. Vacic V, Oldfield CJ, Mohan A, Radivojac P, Cortese MS, Uversky VN, Dunker AK. 2007. Characterization of molecular recognition features, MoRFs, and their binding partners. J. Proteome Res. 6: 2351-2366.
51. Vise PD, Baral B, Latos AJ, Daughdrill GW. 2005. NMR chemical shift and relaxation measurements provide evidence for the coupled folding and binding of the p53 transactivation domain. Nucleic Acids Res. 33: 2061-2077.
52. Wishart DS, Sykes BD. 1994a. The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J. Biomol. NMR 4: 171-180.
53. Wishart DS, Case DA. 2001. Use of chemical shifts in macromolecular structure determination. Methods Enzymol. 338: 3-34.
54. Wishart DS, Sykes BD. 1994b. Chemical shifts as a tool for structure determination. Methods Enzymol. 239: 363-392.
55. Wishart DS, Nip AM. 1998. Protein chemical shift analysis: a practical guide. Biochem. Cell. Biol. 76: 153-163.
56. Wittekind M, Mueller L. 1993. HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins. J. Magn. Reson. B 2: 201-205.