Insights into the Hendra virus NTAIL-XD complex: Evidence for a parallel organization of the helical MoRE at the XD surface stabilized by a combination of hydrophobic and polar interactions

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1854, Issue 8, 2015, Pages 1038-1053

  Erales, Jenny ^a   Beltrandi, Matilde ^a   Roche, Jennifer ^a   Maté, Maria ^a   Longhi, Sonia ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Binding affinity; Far UV circular dichroism; Intrinsically disordered proteins; Isothermal titration calorimetry; Protein protein interactions and interfaces; Small angle X ray scattering

Indexed keywords

INTRINSICALLY DISORDERED PROTEIN; NUCLEOPROTEIN; NUCLEOPROTEIN, HENDRA VIRUS; VIRUS PROTEIN;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; COMPLEX FORMATION; HENDRA VIRUS; HYDRODYNAMICS; HYDROPHOBICITY; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR RECOGNITION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY; X RAY CRYSTALLOGRAPHY; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

HENDRA VIRUS; HENIPAVIRUS; PARAMYXOVIRIDAE;

HENDRA VIRUS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; NUCLEOPROTEINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; VIRAL PROTEINS;

EID: 84930216174     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2015.04.031     Document Type: Article

References (59)

1. L.F. Wang, M. Yu, E. Hansson, L.I. Pritchard, B. Shiell, W.P. Michalski, and B.T. Eaton The exceptionally large genome of Hendra virus: support for creation of a new genus within the family Paramyxoviridae J. Virol. 74 2000 9972 9979
2. G.A. Marsh, C. de Jong, J.A. Barr, M. Tachedjian, C. Smith, D. Middleton, M. Yu, S. Todd, A.J. Foord, V. Haring, J. Payne, R. Robinson, I. Broz, G. Crameri, H.E. Field, and L.F. Wang Cedar virus: a novel Henipavirus isolated from Australian bats PLoS Pathog. 8 2012 e1002836
3. J. Habchi, S. Blangy, L. Mamelli, M. Ringkjobing Jensen, M. Blackledge, H. Darbon, M. Oglesbee, Y. Shu, and S. Longhi Characterization of the interactions between the nucleoprotein and the phosphoprotein of Henipaviruses J. Biol. Chem. 286 2011 13583 13602
4. M. Martinho, J. Habchi, Z. El Habre, L. Nesme, B. Guigliarelli, V. Belle, and S. Longhi Assessing induced folding within the intrinsically disordered C-terminal domain of the Henipavirus nucleoproteins by site directed spin labeling EPR spectroscopy J. Biomol. Struct. Dyn. 31 2013 453 471
5. G. Communie, J. Habchi, F. Yabukarski, D. Blocquel, R. Schneider, N. Tarbouriech, N. Papageorgiou, R.W. Ruigrok, M. Jamin, M. Ringkjøbing-Jensen, S. Longhi, and M. Blackledge Atomic resolution description of the interaction between the nucleoprotein and phosphoprotein of Hendra virus PLoS Pathog. 9 2013 e1003631
6. Y.P. Chan, C.L. Koh, S.K. Lam, and L.F. Wang Mapping of domains responsible for nucleocapsid protein-phosphoprotein interaction of Henipaviruses J. Gen. Virol. 85 2004 1675 1684
7. M. Omi-Furutani, M. Yoneda, K. Fujita, F. Ikeda, and C. Kai Novel phosphoprotein-interacting region in Nipah virus nucleocapsid protein and its involvement in viral replication J. Virol. 84 2010 9793 9799
8. D. Blocquel, J. Habchi, A. Gruet, S. Blangy, and S. Longhi Compaction and binding properties of the intrinsically disordered C-terminal domain of Henipavirus nucleoprotein as unveiled by deletion studies Mol. BioSyst. 8 2012 392 410
9. 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
10. 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
11. A.K. Dunker, C.J. Oldfield, J. Meng, P. Romero, J.Y. Yang, J.W. Chen, V. Vacic, Z. Obradovic, and V.N. Uversky The unfoldomics decade: an update on intrinsically disordered proteins BMC Genomics 9 Suppl. 2 2008 S1
12. A.K. Dunker, I. Silman, V.N. Uversky, and J.L. Sussman Function and structure of inherently disordered proteins Curr. Opin. Struct. Biol. 18 2008 756 764
13. V.N. Uversky The mysterious unfoldome: structureless, underappreciated, yet vital part of any given proteome J. Biomed. Biotechnol. 2010 2010 568068
14. V.N. Uversky, and A.K. Dunker Understanding protein non-folding Biochim. Biophys. Acta 1804 2010 1231 1264
15. K.K. Turoverov, I.M. Kuznetsova, and V.N. Uversky The protein kingdom extended: ordered and intrinsically disordered proteins, their folding, supramolecular complex formation, and aggregation Prog. Biophys. Mol. Biol. 102 2010 73 84
16. T. Chouard Structural biology: breaking the protein rules Nature 471 2011 151 153
17. V.N. Uversky A decade and a half of protein intrinsic disorder: biology still waits for physics Protein Sci. 22 2013 693 724
18. J. Habchi, P. Tompa, S. Longhi, and V.N. Uversky Introducing protein intrinsic disorder Chem. Rev. 114 2014 6561 6588
19. L. Baronti, J. Erales, J. Habchi, I.C. Felli, R. Pierattelli, and S. Longhi Dynamics of the intrinsically disordered C-terminal domain of the Nipah virus nucleoprotein and interaction with the X domain of the phosphoprotein as unveiled by NMR spectroscopy ChemBioChem 16 2015 268 276
20. A. Mohan, C.J. Oldfield, P. Radivojac, V. Vacic, M.S. Cortese, A.K. Dunker, and V.N. Uversky Analysis of molecular recognition features (MoRFs) J. Mol. Biol. 362 2006 1043 1059
21. V. Vacic, C.J. Oldfield, A. Mohan, P. Radivojac, M.S. Cortese, V.N. Uversky, and A.K. Dunker Characterization of molecular recognition features, MoRFs, and their binding partners J. Proteome Res. 6 2007 2351 2366
22. K. Johansson, J.M. Bourhis, V. Campanacci, C. Cambillau, B. Canard, and S. Longhi 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 2003 44567 44573
23. R.L. Kingston, D.J. Hamel, L.S. Gay, F.W. Dahlquist, and B.W. Matthews Structural basis for the attachment of a paramyxoviral polymerase to its template Proc. Natl. Acad. Sci. U. S. A. 101 2004 8301 8306
24. L. Whitmore, and B.A. Wallace DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data Nucleic Acids Res. 32 2004 W668 W673
25. L. Whitmore, and B.A. Wallace Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases Biopolymers 89 2008 392 400
26. V.N. Uversky What does it mean to be natively unfolded? Eur. J. Biochem. 269 2002 2 12
27. S. Brocca, L. Testa, F. Sobott, M. Samalikova, A. Natalello, E. Papaleo, M. Lotti, L. De Gioia, S.M. Doglia, L. Alberghina, and R. Grandori Compaction properties of an intrinsically disordered protein: sic1 and its kinase-inhibitor domain Biophys. J. 100 2011 2243 2252
28. K. Gast, H. Damaschun, R. Misselwitz, M. Muller-Frohne, D. Zirwer, and G. Damaschun Compactness of protein molten globules: temperature-induced structural changes of the apomyoglobin folding intermediate Eur. Biophys. J. 23 1994 297 305
29. D.K. Wilkins, S.B. Grimshaw, V. Receveur, C.M. Dobson, J.A. Jones, and L.J. Smith Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques Biochemistry 38 1999 16424 16431
30. P.V. Konarev, V.V. Volkov, A.V. 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
31. D. Svergun Determination of the regularization parameters in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25 1992 495 503
32. D. Franke, and D.I. Svergun DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering J. Appl. Crystallogr. 42 2009 342 346
33. V.V. Volkov, and D.I. Svergun Uniqueness of ab initio shape determination in small-angle scattering J. Appl. Crystallogr. 36 2003 860 864
34. L.A. Kelley, and M.J. Sternberg Protein structure prediction on the Web: a case study using the Phyre server Nat. Protoc. 4 2009 363 371
35. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
36. W.F. van Gunsteren, S.R. Billeter, A.A. Eising, P.H. Hünenberger, P. Krüger, A.E. Mark, W.R.P. Scott, and I.G. Tironi Biomolecular Simulation: The GROMOS96 Manual and User Guide 1996 vdf Hochschuverlag Zürich, Switzerland
37. S. Ramachandran, P. Kota, F. Ding, and N.V. Dokholyan Automated minimization of steric clashes in protein structures Proteins 79 2011 261 270
38. T.K. Harris, and G.J. Turner Structural basis of perturbed pKa values of catalytic groups in enzyme active sites IUBMB Life 53 2002 85 98
39. V.N. Uversky Natively unfolded proteins: a point where biology waits for physics Protein Sci. 11 2002 739 756
40. P. Tompa Intrinsically unstructured proteins Trends Biochem. Sci. 27 2002 527 533
41. D. Svergun, C. Barberato, and M.H.J. Koch CRYSOL, a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates J. Appl. Crystallogr. 28 1995 768 773
42. R.L. Kingston, L.S. Gay, W.S. Baase, and B.W. Matthews Structure of the nucleocapsid-binding domain from the mumps virus polymerase; an example of protein folding induced by crystallization J. Mol. Biol. 379 2008 719 731
43. K. Yegambaram, E.M. Bulloch, and R.L. Kingston Protein domain definition should allow for conditional disorder Protein Sci. 22 2013 1502 1518
44. A. D'Urzo, A. Konijnenberg, G. Rossetti, J. Habchi, J. Li, P. Carloni, F. Sobott, S. Longhi, and R. Grandori Molecular basis for structural heterogeneity of an intrinsically disordered protein bound to a partner by combined ESI-IM-MS and modeling J. Am. Soc. Mass Spectrom. 26 2015 472 481
45. P. Tompa, and M. Fuxreiter Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions Trends Biochem. Sci. 33 2008 2 8
46. A. Bhattacherjee, and S. Wallin Coupled folding-binding in a hydrophobic/polar protein model: impact of synergistic folding and disordered flanks Biophys. J. 102 2012 569 578
47. M. Fuxreiter Fuzziness: linking regulation to protein dynamics Mol. BioSyst. 8 2012 168 177
48. M. Ringkjøbing Jensen, G. Communie, E.D. Ribeiro Jr., N. Martinez, A. Desfosses, L. Salmon, L. Mollica, F. Gabel, M. Jamin, S. Longhi, R.W. Ruigrok, and M. Blackledge Intrinsic disorder in measles virus nucleocapsids Proc. Natl. Acad. Sci. U. S. A. 108 2011 9839 9844
49. S.A. Krumm, M. Takeda, and R.K. Plemper The measles virus nucleocapsid protein tail domain is dispensable for viral polymerase recruitment and activity J. Biol. Chem. 288 2013 29943 29953
50. B. Meszaros, P. Tompa, I. Simon, and Z. Dosztanyi Molecular principles of the interactions of disordered proteins J. Mol. Biol. 372 2007 549 561
51. K. Houben, D. Marion, N. Tarbouriech, R.W. Ruigrok, and L. Blanchard 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 2007 6807 6816
52. G. Schreiber, G. Haran, and H.X. Zhou Fundamental aspects of protein-protein association kinetics Chem. Rev. 109 2009 839 860
53. Y. Xue, T. Yuwen, F. Zhu, and N.R. Skrynnikov Role of electrostatic interactions in binding of peptides and intrinsically disordered proteins to their folded targets. 1. NMR and MD characterization of the complex between the c-Crk N-SH3 domain and the peptide Sos Biochemistry 53 2014 6473 6495
54. E.T. Wong, D. Na, and J. Gsponer On the importance of polar interactions for complexes containing intrinsically disordered proteins PLoS Comput. Biol. 9 2013 e1003192
55. D. Ganguly, S. Otieno, B. Waddell, L. Iconaru, R.W. Kriwacki, and J. Chen Electrostatically accelerated coupled binding and folding of intrinsically disordered proteins J. Mol. Biol. 422 2012 674 684
56. D. Ganguly, W. Zhang, and J. Chen Electrostatically accelerated encounter and folding for facile recognition of intrinsically disordered proteins PLoS Comput. Biol. 9 2013 e1003363
57. D. Blocquel, J.M. Bourhis, J.F. Eléouët, D. Gerlier, J. Habchi, M. Jamin, S. Longhi, and F. Yabukarski Transcription et réplication des Mononégavirales: une machine moléculaire originale Virologie 16 2012 225 257
58. J. Habchi, and S. Longhi Structural disorder within paramyxovirus nucleoproteins and phosphoproteins Mol. BioSyst. 8 2012 69 81
59. J. Habchi, L. Mamelli, and S. Longhi Structural disorder within the nucleoprotein and phosphoprotein from measles, Nipah and Hendra viruses V.N. Uversky, S. Longhi, Flexible Viruses: Structural Disorder in Viral Proteins 2012 John Wiley and Sons Hoboken, New Jersey 47 94