Assessing induced folding within the intrinsically disordered C-terminal domain of the Henipavirus nucleoproteins by site-directed spin labeling EPR spectroscopy

Journal of Biomolecular Structure and Dynamics

Volumn 31, Issue 5, 2013, Pages 453-471

  Martinho, Marlène ^a   Habchi, Johnny ^a   El Habre, Zeina ^a   Nesme, Léo ^a   Guigliarelli, Bruno ^a   Belle, Valérie ^a   Longhi, Sonia ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

EPR spectroscopy; Hendra; Induced folding; Intrinsic disorder; Nipah; Nucleoprotein; Phosphoprotein; Spin labeling

Indexed keywords

PHOSPHOPROTEIN; VIRUS NUCLEOPROTEIN;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; COMPLEX FORMATION; ELECTRON SPIN RESONANCE; HENDRA VIRUS; HENIPAVIRUS; LIGHT SCATTERING; MEASLES VIRUS; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NIPAH VIRUS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN PURIFICATION; REFRACTOMETRY; SPIN LABELING; ULTRAVIOLET SPECTROSCOPY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CIRCULAR DICHROISM; ELECTRON SPIN RESONANCE SPECTROSCOPY; HENDRA VIRUS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NIPAH VIRUS; NUCLEOPROTEINS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; VIRAL PROTEINS;

HENDRA VIRUS; HENIPAVIRUS; MEASLES VIRUS; NIPAH VIRUS;

EID: 84879206318     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2012.706068     Document Type: Article

References (69)

1. Belle, V., Rouger, S., Costanzo, S., Liquiere, E., Strancar, J., Guigliarelli, B., ...Longhi, S. (2008). Mapping alphahelical induced folding within the intrinsically disordered C-terminal domain of the measles virus nucleoprotein by site-directed spin-labeling EPR spectroscopy. Proteins: Structure, Function and Bioinformatics, 73, 973-988.
2. Belle, V., Rouger, S., Costanzo, S., Longhi, S., & Fournel, A. (2010). Site-directed spin labeling EPR spectroscopy. In V. N. Uversky & S. Longhi (Eds.), Instrumental analysis of intrinsically disordered proteins: Assessing structure and conformation. Hoboken, NJ: Wiley.
3. Biswas, R., Kuhne, H., Brudvig, G.W., & Gopalan, V. (2001). Use of EPR spectroscopy to study macromolecular structure and function. Science Progress, 84, 45-67.
4. Blocquel, D., Habchi, J., Gruet, A., Blangy, S., & Longhi, S. (2012). Compaction and binding properties of the intrinsically disordered C-terminal domain of Henipavirus nucleoprotein as unveiled by deletion studies. Molecular BioSystems, 8, 392-410.
5. Bourhis, J.M., Receveur-Bréchot, V., Oglesbee, M., Zhang, X., Buccellato, M., Darbon, H., ...Longhi, S. (2005). 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 Science, 14, 1975-1992.
6. Bridges, M.D., Hideg, K., & Hubbell, W.L. (2010). Resolving conformational and rotameric exchange in spin-labeled proteins using saturation recovery EPR. Applied Magnetic Resonance, 37, 363.
7. Bryson, K., McGuffin, L.J., Marsden, R.L., Ward, J.J., Sodhi, J.S., & Jones, D.T. (2005). Protein structure prediction servers at University College London. Nucleic Acids Research, 33, W36-W38.
8. Chan, Y.P., Koh, C.L., Lam, S.K., & Wang, L.F. (2004). Mapping of domains responsible for nucleocapsid protein-phosphoprotein interaction of Henipaviruses. Journal of General Virology, 85, 1675-1684.
9. Chouard, T. (2011). Structural biology: Breaking the protein rules. Nature, 471, 151-153.
10. DeLano, W.L. (2002). The PyMOL molecular graphics system. Proteins: Structure, Function and Bioinformatics, 30, 442-454.
11. Drescher, M. (2012). EPR in protein science: Intrinsically disordered proteins. Topics in Current Chemistry, 321, 91-119.
12. Dunker, A.K., Cortese, M.S., Romero, P., Iakoucheva, L.M., & Uversky, V.N. (2005). Flexible nets. FEBS Journal, 272, 5129-5148.
13. Dunker, A.K., Lawson, J.D., Brown, C.J., Williams, R.M., Romero, P., Oh, J.S., ...Obradovic, Z. (2001). Intrinsically disordered protein. Journal of Molecular Graphics and Modelling, 19, 26-59.
14. Dunker, A.K., & Obradovic, Z. (2001). The protein trinity - Linking function and disorder. Nature Biotechnology, 19, 805-806.
15. Dunker, A.K., Oldfield, C.J., Meng, J., Romero, P., Yang, J.Y., Chen, J.W., ...Uversky, V.N. (2008). The unfoldomics decade: An update on intrinsically disordered proteins. BMC Genomics, 9(Suppl. 2), S1.
16. Dunker, A.K., Silman, I., Uversky, V.N., & Sussman, J.L. (2008). Function and structure of inherently disordered proteins. Current Opinion in Structural Biology, 18, 756-764.
17. Dyson, H.J., & Wright, P.E. (2002). Coupling of folding and binding for unstructured proteins. Current Opinion in Structural Biology, 12, 54-60.
18. Dyson, H.J., & Wright, P.E. (2005). Intrinsically unstructured proteins and their functions. Nature Reviews Molecular Cell Biology, 6, 197-208.
19. Eaton, B.T., Mackenzie, J.S., & Wang, L.F. (2007). Henipaviruses. In B.N. Fields, D.M. Knipe, & P.M. Howley (Eds.), Fields virology (pp. 1587-1600). Philadelphia, PA: Lippincott- Raven.
20. Erales, J., Lorenzi, M., Lebrun, R., Fournel, A., Etienne, E., Courcelle, C., ...Belle, V. (2009). A new function of GAPDH from Chlamydomonas reinhardtii: A thiol-disulfide exchange reaction with CP12. Biochemistry, 48, 6034-6040.
21. Fanucci, G.E., & Cafiso, D.S. (2006). Recent advances and applications of site-directed spin labeling. Current Opinion in Structural Biology, 16, 644-653.
22. Feix, J.B., & Klug, C.S. (1998). Site-directed spin-labeling of membrane proteins and peptide-membrane interactions. In L. Berliner (Ed.). Biological magnetic resonance. Spin labeling: the next millennium (pp. 251-281). New York, NY: Plenum Press.
23. Fuxreiter, M., Simon, I., Friedrich, P., & Tompa, P. (2004). Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. Journal of Molecular Biology, 338, 1015-1026.
24. Fuxreiter, M., Tompa, P., & Simon, I. (2007). Local structural disorder imparts plasticity on linear motifs. Bioinformatics, 23, 950-956.
25. Guo, Z., Cascio, D., Hideg, K., & Hubbell, W.L. (2008). Structural determinants of nitroxide motion in spin-labeled proteins: solvent-exposed sites in helix B of T4 lysozyme. Protein Science, 17, 228-239.
26. Guo, Z., Cascio, D., Hideg, K., Kalai, T., & Hubbell, W.L. (2007). Structural determinants of nitroxide motion in spinlabeled proteins: tertiary contact and solvent-inaccessible sites in helix G of T4 lysozyme. Protein Science, 16, 1069-1086.
27. Habchi, J., Mamelli, L., & Longhi, S. (2012). Structural disorder within the nucleoprotein and phosphoprotein from measles, Nipah and Hendra viruses. In V.N. Uversky & S. Longhi (Eds.), Flexible viruses: Structural disorder in viral proteins. Hoboken, NJ: Wiley.
28. Habchi, J., Blangy, S., Mamelli, L., Ringkjobing Jensen, M., Blackledge, M., Darbon, H., ...Longhi, S. (2011). Characterization of the interactions between the nucleoprotein and the phosphoprotein of Henipaviruses. Journal of Biological Chemistry, 286, 13583-13602.
29. Habchi, J., & Longhi, S. (2012). Structural disorder within paramyxovirus nucleoproteins and phosphoproteins. Molecular BioSystems, 8, 69-81.
30. Habchi, J., Mamelli, L., Darbon, H., & Longhi, S. (2010). Structural disorder within henipavirus nucleoprotein and phosphoprotein: From predictions to experimental assessment. PLoS One, 5, e11684.
31. Hua, Q.X., Jia, W.H., Bullock, B.P., Habener, J.F., & Weiss, M.A. (1998). Transcriptional activator-coactivator recognition: Nascent folding of a kinase-inducible transactivation domain predicts its structure on coactivator binding. Biochemistry, 37, 5858-5866.
32. Hubbell, W.L., Altenbach, C., Hubbell, C.M., & Khorana, H.G. (2003). Rhodopsin structure, dynamics, and activation: a perspective from crystallography, site-directed spin labeling, sulfhydryl reactivity, and disulfide cross-linking. Advances in Protein Chemistry, 63, 243-290.
33. Hubbell, W.L., McHaourab, H.S., Altenbach, C., & Lietzow, M.A. (1996). Watching proteins move using site-directed spin labeling. Structure, 4, 779-783.
34. Johansson, K., Bourhis, J.M., 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. Journal of Biological Chemistry, 278, 44567-44573.
35. Kavalenka, A., Urbancic, I., Belle, V., Rouger, S., Costanzo, S., Kure, S., ...Strancar, J. (2010). Conformational analysis of the partially disordered measles virus NTAIL-XD complex by SDSL EPR spectroscopy. Biophysical Journal, 98, 1055-1064.
36. Kingston, R.L., Hamel, D.J., Gay, L.S., Dahlquist, F.W., & Matthews, B.W. (2004). Structural basis for the attachment of a paramyxoviral polymerase to its template. Proceedings of the National Academy of Sciences of the United States of America, 101, 8301-8306.
37. Klare, J.P., & Steinhoff, H.J. (2009). Spin labeling EPR. Photosynthesis Research, 102, 377-390.
38. Kriwacki, R.W., Hengst, L., Tennant, L., Reed, S.I., & Wright, P. E. (1996). Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity. Proceedings of the National Academy of Sciences of the United States of America, 93, 11504-11509.
39. Lacy, E.R., Filippov, I., Lewis, W.S., Otieno, S., Xiao, L., Weiss, S., ...Kriwacki, R.W. (2004). P27 binds cyclin- CDK complexes through a sequential mechanism involving binding-induced protein folding. Nature Structural & Molecular Biology, 11, 358-364.
40. Langen, R., Oh, K.J., Cascio, D., & Hubbell, W.L. (2000). Crystal structures of spin labeled T4 lysozyme mutants: Implications for the interpretation of EPR spectra in terms of structure. Biochemistry, 39, 8396-8405.
41. Longhi, S., Belle, V., Fournel, A., Guigliarelli, B., & Carrière, F. (2011). Probing structural transitions in both structured and disordered proteins by site-directed spin-labeling EPR spectroscopy. Journal of Peptide Science, 17, 315-328.
42. Lorenzi, M., Puppo, C., Lebrun, R., Lignon, S., Roubaud, V., Martinho, M., ...Belle, V. (2011). Tyrosine-targeted spin labeling and EPR spectroscopy: An alternative strategy for studying structural transitions in proteins. Angewandte Chemie (International ed. in English), 50, 9108-9111.
43. McHaourab, H.S., Lietzow, M.A., Hideg, K., & Hubbell, W.L. (1996). Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry, 35, 7692-7704.
44. Mohan, A., Oldfield, C.J., Radivojac, P., Vacic, V., Cortese, M. S., Dunker, A.K., & Uversky, V.N. (2006). Analysis of molecular recognition features (MoRFs). Journal of Molecular Biology, 362, 1043-1059.
45. Morin, B., Bourhis, J.M., Belle, V., Woudstra, M., Carrière, F., Guigliarelli, B., ...Longhi, S. (2006). Assessing induced folding of an intrinsically disordered protein by site-directed spin-labeling EPR spectroscopy. Journal of Physical Chemistry B, 110, 20596-20608.
46. Oldfield, C.J., Cheng, Y., Cortese, M.S., Romero, P., Uversky, V.N., & Dunker, A.K. (2005). Coupled folding and binding with alpha-helix-forming molecular recognition elements. Biochemistry, 44, 12454-12470.
47. Omi-Furutani, M., Yoneda, M., Fujita, K., Ikeda, F., & Kai, C. (2010). Novel phosphoprotein-interacting region in Nipah virus nucleocapsid protein and its involvement in viral replication. Journal of Virology, 84, 9793-9799.
48. Pirman, N.L., Milshteyn, E., Galiano, L., Hewlett, J.C., & Fanucci, G.E. (2011). Characterization of the disordered-toalpha- helical transition of IA by SDSL-EPR spectroscopy. Protein Science, 20, 150-159.
49. Polyhach, Y., Bordignon, E., & Jeschke, G. (2011). Rotamer libraries of spin labelled cysteines for protein studies. Physical Chemistry Chemical Physics, 13, 2356-2366.
50. Radivojac, P., Iakoucheva, L.M., Oldfield, C.J., Obradovic, Z., Uversky, V.N., & Dunker, A.K. (2007). Intrinsic disorder and functional proteomics. Biophysical Journal, 92, 1439-1456.
51. Ranaldi, S., Belle, V., Woudstra, M., Bourgeas, R., Guigliarelli, B., Roche, P., ...Fournel, A. (2010). Amplitude of pancreatic lipase lid opening in solution and identification of spin label conformational subensembles by combining continuous wave and pulsed EPR spectroscopy and molecular dynamics. Biochemistry, 49, 2140-2149.
52. Ringkjøbing Jensen, M., Communie, G., Ribeiro, E.D. Jr., Martinez, N., Desfosses, A., Salmon, L., ...Blackledge, M. (2011). Intrinsic disorder in measles virus nucleocapsids. Proceedings of the National Academy of Sciences of the United States of America, 108, 9839-9844.
53. Sivakolundu, S.G., Bashford, D., & Kriwacki, R.W. (2005). Disordered p27Kip1 exhibits intrinsic structure resembling the Cdk2/cyclin A-bound conformation. Journal of Molecular Biology, 353, 1118-1128.
54. Strancar, J., Koklic, T., Arsov, Z., Filipic, B., Stopar, D., & Hemminga, M.A. (2005). Spin label EPR-based characterization of biosystem complexity. Journal of Chemical Information and Modeling, 45, 394-406.
55. Timofeev, V.P., & Tsetlin, V.I. (1983). Analysis of mobility of protein side chains by spin-label technique. Biophysics of Structure and Mechanisms, 10, 93-108.
56. Tompa, P. (2002). Intrinsically unstructured proteins. Trends in Biochemical Science, 27, 527-533.
57. Tompa, P., & Fuxreiter, M. (2008). Fuzzy complexes: Polymorphism and structural disorder in protein-protein interactions. Trends in Biochemical Science, 33, 2-8.
58. Tsai, C.D., Ma, B., Kumar, S., Wolfson, H., & Nussinov, R. (2001). Protein folding: binding of conformationally fluctuating building blocks via population selection. Critical Reviews in Biochemistry and Molecular Biology, 36, 399-433.
59. Tsai, C.J., Ma, B., Sham, Y.Y., Kumar, S., & Nussinov, R. (2001). Structured disorder and conformational selection. Proteins: Structure, Function and Bioinformatics, 44, 418-427.
60. Turoverov, K.K., Kuznetsova, I.M., & Uversky, V.N. (2010). The protein kingdom extended: Ordered and intrinsically disordered proteins, their folding, supramolecular complex formation, and aggregation. Progress in Biophysics & Molecular Biology, 102, 73-84.
61. Uversky, V.N. (1993). Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule. Biochemistry, 32, 13288-13298.
62. Uversky, V.N. (2002a). Natively unfolded proteins: A point where biology waits for physics. Protein Science, 11, 739-756.
63. Uversky, V.N. (2002b). What does it mean to be natively unfolded? European Journal of Biochemistry, 269, 2-12.
64. Uversky, V.N. (2003). Protein folding revisited. A polypeptide chain at the folding-misfolding-nonfolding cross-roads: Which way to go? Cellular and Molecular Life Sciences, 60, 1852-1871.
65. Uversky, V.N. (2010). The mysterious unfoldome: Structureless, underappreciated, yet vital part of any given proteome. Journal of Biomedicine and Biotechnology, 2010, 568068.
66. Uversky, V.N., & Dunker, A.K. (2010). Understanding protein non-folding. Biochimica et Biophysica Acta, 1804, 1231-1264.
67. Uversky, V.N., Oldfield, C.J., & Dunker, A.K. (2005). Showing your ID: Intrinsic disorder as an ID for recognition, regulation and cell signaling. Journal of Molecular Recognition, 18, 343-384.
68. Vacic, V., Oldfield, C.J., Mohan, A., Radivojac, P., Cortese, M. S., Uversky, V.N., & Dunker, A.K. (2007). Characterization of molecular recognition features, MoRFs, and their binding partners. Journal of Proteome Research, 6, 2351-2366.
69. Wang, L.F., Yu, M., Hansson, E., Pritchard, L.I., Shiell, B., Michalski, W.P., & Eaton, B.T. (2000). The exceptionally large genome of Hendra virus: Support for creation of a new genus within the family Paramyxoviridae. Journal of Virology, 74, 9972-9979.