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

References

• Belle , V. , Rouger , S. , Costanzo , S. , Liquiere , E. , Strancar , J. , Guigliarelli , B. , … and 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: Structure, Function and Bioinformatics , 73 : 973 – 988 .
   PubMed Web of Science ®Google Scholar
• Belle , V. , Rouger , S. , Costanzo , S. , Longhi , S. and Fournel , A. 2010 . “ Site-directed spin labeling EPR spectroscopy ” . In Instrumental analysis of intrinsically disordered proteins: Assessing structure and conformation , Edited by: Uversky , V.N. and Longhi , S. Hoboken , NJ : Wiley .
   Google Scholar
• Biswas , R. , Kuhne , H. , Brudvig , G.W. and Gopalan , V. 2001 . Use of EPR spectroscopy to study macromolecular structure and function . Science Progress , 84 : 45 – 67 .
   PubMedGoogle Scholar
• Blocquel , D. , Habchi , J. , Gruet , A. , Blangy , S. and 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 .
   PubMedGoogle Scholar
• Bourhis , J.M. , Receveur-Bréchot , V. , Oglesbee , M. , Zhang , X. , Buccellato , M. , Darbon , H. , … and 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 .
   PubMed Web of Science ®Google Scholar
• Bridges , M.D. , Hideg , K. and Hubbell , W.L. 2010 . Resolving conformational and rotameric exchange in spin-labeled proteins using saturation recovery EPR . Applied Magnetic Resonance , 37 : 363
   PubMed Web of Science ®Google Scholar
• Bryson , K. , McGuffin , L.J. , Marsden , R.L. , Ward , J.J. , Sodhi , J.S. and Jones , D.T. 2005 . Protein structure prediction servers at University College London . Nucleic Acids Research , 33 : W36 – W38 .
   PubMed Web of Science ®Google Scholar
• Chan , Y.P. , Koh , C.L. , Lam , S.K. and Wang , L.F. 2004 . Mapping of domains responsible for nucleocapsid protein–phosphoprotein interaction of Henipaviruses . Journal of General Virology , 85 : 1675 – 1684 .
   PubMed Web of Science ®Google Scholar
• Chouard , T. 2011 . Structural biology: Breaking the protein rules . Nature , 471 : 151 – 153 .
   PubMed Web of Science ®Google Scholar
• DeLano , W.L. 2002 . The PyMOL molecular graphics system . Proteins: Structure, Function and Bioinformatics , 30 : 442 – 454 .
   Google Scholar
• Drescher, M. (2012). EPR in protein science: Intrinsically disordered proteins. Topics in Current Chemistry, 321, 91–119.
   Google Scholar
• Dunker , A.K. , Cortese , M.S. , Romero , P. , Iakoucheva , L.M. and Uversky , V.N. 2005 . Flexible nets . FEBS Journal , 272 : 5129 – 5148 .
   PubMed Web of Science ®Google Scholar
• Dunker , A.K. , Lawson , J.D. , Brown , C.J. , Williams , R.M. , Romero , P. , Oh , J.S. , … and Obradovic , Z. 2001 . Intrinsically disordered protein . Journal of Molecular Graphics and Modelling , 19 : 26 – 59 .
   PubMed Web of Science ®Google Scholar
• Dunker , A.K. and Obradovic , Z. 2001 . The protein trinity – Linking function and disorder . Nature Biotechnology , 19 : 805 – 806 .
   PubMed Web of Science ®Google Scholar
• Dunker , A.K. , Oldfield , C.J. , Meng , J. , Romero , P. , Yang , J.Y. , Chen , J.W. , … and Uversky , V.N. 2008 . The unfoldomics decade: An update on intrinsically disordered proteins . BMC Genomics , 9 ( Suppl. 2 ) : S1
   PubMed Web of Science ®Google Scholar
• Dunker , A.K. , Silman , I. , Uversky , V.N. and Sussman , J.L. 2008 . Function and structure of inherently disordered proteins . Current Opinion in Structural Biology , 18 : 756 – 764 .
   PubMed Web of Science ®Google Scholar
• Dyson , H.J. and Wright , P.E. 2002 . Coupling of folding and binding for unstructured proteins . Current Opinion in Structural Biology , 12 : 54 – 60 .
   PubMed Web of Science ®Google Scholar
• Dyson , H.J. and Wright , P.E. 2005 . Intrinsically unstructured proteins and their functions . Nature Reviews Molecular Cell Biology , 6 : 197 – 208 .
   PubMed Web of Science ®Google Scholar
• Eaton , B.T. , Mackenzie , J.S. and Wang , L.F. 2007 . “ Henipaviruses ” . In Fields virology , Edited by: Fields , B.N. , Knipe , D.M. and Howley , P.M. 1587 – 1600 . Philadelphia , PA : Lippincott-Raven .
   Google Scholar
• Erales , J. , Lorenzi , M. , Lebrun , R. , Fournel , A. , Etienne , E. , Courcelle , C. , … and Belle , V. 2009 . A new function of GAPDH from Chlamydomonas reinhardtii: A thiol-disulfide exchange reaction with CP12 . Biochemistry , 48 : 6034 – 6040 .
   PubMed Web of Science ®Google Scholar
• Fanucci , G.E. and Cafiso , D.S. 2006 . Recent advances and applications of site-directed spin labeling . Current Opinion in Structural Biology , 16 : 644 – 653 .
   PubMed Web of Science ®Google Scholar
• 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.
   Google Scholar
• Fuxreiter , M. , Simon , I. , Friedrich , P. and Tompa , P. 2004 . Preformed structural elements feature in partner recognition by intrinsically unstructured proteins . Journal of Molecular Biology , 338 : 1015 – 1026 .
   PubMed Web of Science ®Google Scholar
• Fuxreiter , M. , Tompa , P. and Simon , I. 2007 . Local structural disorder imparts plasticity on linear motifs . Bioinformatics , 23 : 950 – 956 .
   PubMed Web of Science ®Google Scholar
• Guo , Z. , Cascio , D. , Hideg , K. and 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 .
   PubMed Web of Science ®Google Scholar
• Guo , Z. , Cascio , D. , Hideg , K. , Kalai , T. and Hubbell , W.L. 2007 . Structural determinants of nitroxide motion in spin-labeled proteins: tertiary contact and solvent-inaccessible sites in helix G of T4 lysozyme . Protein Science , 16 : 1069 – 1086 .
   PubMed Web of Science ®Google Scholar
• Habchi , J. , Mamelli , L. and Longhi , S. 2012 . “ Structural disorder within the nucleoprotein and phosphoprotein from measles, Nipah and Hendra viruses ” . In Flexible viruses: Structural disorder in viral proteins , Edited by: Uversky , V.N. and Longhi , S. Hoboken , NJ : Wiley .
   Google Scholar
• Habchi , J. , Blangy , S. , Mamelli , L. , Ringkjobing Jensen , M. , Blackledge , M. , Darbon , H. , … and Longhi , S. 2011 . Characterization of the interactions between the nucleoprotein and the phosphoprotein of Henipaviruses . Journal of Biological Chemistry , 286 : 13583 – 13602 .
   PubMed Web of Science ®Google Scholar
• Habchi , J. and Longhi , S. 2012 . Structural disorder within paramyxovirus nucleoproteins and phosphoproteins . Molecular BioSystems , 8 : 69 – 81 .
   PubMedGoogle Scholar
• Habchi , J. , Mamelli , L. , Darbon , H. and Longhi , S. 2010 . Structural disorder within henipavirus nucleoprotein and phosphoprotein: From predictions to experimental assessment . PLoS One , 5 : e11684
   PubMed Web of Science ®Google Scholar
• Hua , Q.X. , Jia , W.H. , Bullock , B.P. , Habener , J.F. and 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 .
   PubMed Web of Science ®Google Scholar
• Hubbell , W.L. , Altenbach , C. , Hubbell , C.M. and 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 .
   PubMedGoogle Scholar
• Hubbell , W.L. , McHaourab , H.S. , Altenbach , C. and Lietzow , M.A. 1996 . Watching proteins move using site-directed spin labeling . Structure , 4 : 779 – 783 .
   PubMed Web of Science ®Google Scholar
• Johansson , K. , Bourhis , J.M. , Campanacci , V. , Cambillau , C. , Canard , B. and 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 .
   PubMed Web of Science ®Google Scholar
• Kavalenka , A. , Urbancic , I. , Belle , V. , Rouger , S. , Costanzo , S. , Kure , S. , … and Strancar , J. 2010 . Conformational analysis of the partially disordered measles virus NTAIL-XD complex by SDSL EPR spectroscopy . Biophysical Journal , 98 : 1055 – 1064 .
   PubMed Web of Science ®Google Scholar
• Kingston , R.L. , Hamel , D.J. , Gay , L.S. , Dahlquist , F.W. and 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 .
   PubMed Web of Science ®Google Scholar
• Klare , J.P. and Steinhoff , H.J. 2009 . Spin labeling EPR . Photosynthesis Research , 102 : 377 – 390 .
   PubMed Web of Science ®Google Scholar
• Kriwacki , R.W. , Hengst , L. , Tennant , L. , Reed , S.I. and 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 .
   PubMed Web of Science ®Google Scholar
• Lacy , E.R. , Filippov , I. , Lewis , W.S. , Otieno , S. , Xiao , L. , Weiss , S. , … and 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 .
   PubMed Web of Science ®Google Scholar
• Langen , R. , Oh , K.J. , Cascio , D. and 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 .
   PubMed Web of Science ®Google Scholar
• Longhi , S. , Belle , V. , Fournel , A. , Guigliarelli , B. and 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 .
   PubMed Web of Science ®Google Scholar
• Lorenzi , M. , Puppo , C. , Lebrun , R. , Lignon , S. , Roubaud , V. , Martinho , M. , … and 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 .
   PubMed Web of Science ®Google Scholar
• McHaourab , H.S. , Lietzow , M.A. , Hideg , K. and Hubbell , W.L. 1996 . Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics . Biochemistry , 35 : 7692 – 7704 .
   PubMed Web of Science ®Google Scholar
• Mohan , A. , Oldfield , C.J. , Radivojac , P. , Vacic , V. , Cortese , M.S. , Dunker , A.K. and Uversky , V.N. 2006 . Analysis of molecular recognition features (MoRFs) . Journal of Molecular Biology , 362 : 1043 – 1059 .
   PubMed Web of Science ®Google Scholar
• Morin , B. , Bourhis , J.M. , Belle , V. , Woudstra , M. , Carrière , F. , Guigliarelli , B. , … and 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 .
   PubMed Web of Science ®Google Scholar
• Oldfield , C.J. , Cheng , Y. , Cortese , M.S. , Romero , P. , Uversky , V.N. and Dunker , A.K. 2005 . Coupled folding and binding with alpha-helix-forming molecular recognition elements . Biochemistry , 44 : 12454 – 12470 .
   PubMed Web of Science ®Google Scholar
• Omi-Furutani , M. , Yoneda , M. , Fujita , K. , Ikeda , F. and Kai , C. 2010 . Novel phosphoprotein-interacting region in Nipah virus nucleocapsid protein and its involvement in viral replication . Journal of Virology , 84 : 9793 – 9799 .
   PubMed Web of Science ®Google Scholar
• Pirman , N.L. , Milshteyn , E. , Galiano , L. , Hewlett , J.C. and Fanucci , G.E. 2011 . Characterization of the disordered-to-alpha-helical transition of IA by SDSL-EPR spectroscopy . Protein Science , 20 : 150 – 159 .
   PubMed Web of Science ®Google Scholar
• Polyhach , Y. , Bordignon , E. and Jeschke , G. 2011 . Rotamer libraries of spin labelled cysteines for protein studies . Physical Chemistry Chemical Physics , 13 : 2356 – 2366 .
   PubMed Web of Science ®Google Scholar
• Radivojac , P. , Iakoucheva , L.M. , Oldfield , C.J. , Obradovic , Z. , Uversky , V.N. and Dunker , A.K. 2007 . Intrinsic disorder and functional proteomics . Biophysical Journal , 92 : 1439 – 1456 .
   PubMed Web of Science ®Google Scholar
• Ranaldi , S. , Belle , V. , Woudstra , M. , Bourgeas , R. , Guigliarelli , B. , Roche , P. , … and 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 .
   PubMed Web of Science ®Google Scholar
• Ringkjøbing Jensen , M. , Communie , G. , Ribeiro , E.D. Jr. , Martinez , N. , Desfosses , A. , Salmon , L. , … and 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 .
   PubMed Web of Science ®Google Scholar
• Sivakolundu , S.G. , Bashford , D. and Kriwacki , R.W. 2005 . Disordered p27Kip1 exhibits intrinsic structure resembling the Cdk2/cyclin A-bound conformation . Journal of Molecular Biology , 353 : 1118 – 1128 .
   PubMed Web of Science ®Google Scholar
• Strancar , J. , Koklic , T. , Arsov , Z. , Filipic , B. , Stopar , D. and Hemminga , M.A. 2005 . Spin label EPR-based characterization of biosystem complexity . Journal of Chemical Information and Modeling , 45 : 394 – 406 .
   PubMed Web of Science ®Google Scholar
• Timofeev , V.P. and Tsetlin , V.I. 1983 . Analysis of mobility of protein side chains by spin-label technique . Biophysics of Structure and Mechanisms , 10 : 93 – 108 .
   Google Scholar
• Tompa , P. 2002 . Intrinsically unstructured proteins . Trends in Biochemical Science , 27 : 527 – 533 .
   PubMed Web of Science ®Google Scholar
• Tompa , P. and Fuxreiter , M. 2008 . Fuzzy complexes: Polymorphism and structural disorder in protein–protein interactions . Trends in Biochemical Science , 33 : 2 – 8 .
   PubMed Web of Science ®Google Scholar
• Tsai , C.D. , Ma , B. , Kumar , S. , Wolfson , H. and Nussinov , R. 2001 . Protein folding: binding of conformationally fluctuating building blocks via population selection . Critical Reviews in Biochemistry and Molecular Biology , 36 : 399 – 433 .
   PubMed Web of Science ®Google Scholar
• Tsai , C.J. , Ma , B. , Sham , Y.Y. , Kumar , S. and Nussinov , R. 2001 . Structured disorder and conformational selection . Proteins: Structure, Function and Bioinformatics , 44 : 418 – 427 .
   PubMed Web of Science ®Google Scholar
• Turoverov , K.K. , Kuznetsova , I.M. and 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 .
   PubMed Web of Science ®Google Scholar
• 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 .
   PubMed Web of Science ®Google Scholar
• Uversky , V.N. 2002a . Natively unfolded proteins: A point where biology waits for physics . Protein Science , 11 : 739 – 756 .
   PubMed Web of Science ®Google Scholar
• Uversky , V.N. 2002b . What does it mean to be natively unfolded? . European Journal of Biochemistry , 269 : 2 – 12 .
   PubMedGoogle Scholar
• 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 .
   PubMed Web of Science ®Google Scholar
• Uversky , V.N. 2010 . The mysterious unfoldome: Structureless, underappreciated, yet vital part of any given proteome . Journal of Biomedicine and Biotechnology , 2010 : 568068
   PubMedGoogle Scholar
• Uversky , V.N. and Dunker , A.K. 2010 . Understanding protein non-folding . Biochimica et Biophysica Acta , 1804 : 1231 – 1264 .
   PubMed Web of Science ®Google Scholar
• Uversky , V.N. , Oldfield , C.J. and 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 .
   PubMed Web of Science ®Google Scholar
• Vacic , V. , Oldfield , C.J. , Mohan , A. , Radivojac , P. , Cortese , M.S. , Uversky , V.N. and Dunker , A.K. 2007 . Characterization of molecular recognition features, MoRFs, and their binding partners . Journal of Proteome Research , 6 : 2351 – 2366 .
   PubMed Web of Science ®Google Scholar
• Wang , L.F. , Yu , M. , Hansson , E. , Pritchard , L.I. , Shiell , B. , Michalski , W.P. and 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 .
   PubMed Web of Science ®Google Scholar