Structural disorder within the measles virus nucleoprotein and phosphoprotein

Protein and Peptide Letters

Volumn 17, Issue 8, 2010, Pages 961-978

  Longhi, Sonia ^a   Oglesbee, Michael ^b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Induced folding; Measles virus; Nucleocapsid; Nucleoprotein; Phosphoprotein; Structural disorder

Indexed keywords

MEASLES VIRUS;

NUCLEAR PROTEIN; NUCLEOPROTEIN; NUCLEOPROTEIN, MEASLES VIRUS; PHOSPHOPROTEIN; VIRUS PROTEIN;

ANIMAL; CHEMISTRY; GENETIC TRANSCRIPTION; GENETICS; HUMAN; MEASLES VIRUS; PHYSIOLOGY; VIRUS REPLICATION;

ANIMALS; HUMANS; MEASLES VIRUS; NUCLEAR PROTEINS; NUCLEOPROTEINS; PHOSPHOPROTEINS; TRANSCRIPTION, GENETIC; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 77956596750     PISSN: 09298665     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986610791498894     Document Type: Review

References (162)

1. Bitko, V.; Barik, S. Phenotypic silencing of cytoplasmic genes using sequence-specific double-stranded short interfering RNA and its application in the reverse genetics of wild type negative-strand RNA viruses. BMC Microbiol., 2001, 1, 34.
2. Plumet, S.; Duprex, W.P.; Gerlier, D. Dynamics of viral RNA synthesis during measles virus infection. J. Virol., 2005, 79, 6900-6908.
3. Longhi, S.; Canard, B. Mécanismes de transcription et de réplication des Paramyxoviridae. Virologie, 1999, 3, 227-240.
4. Lamb, R.A.; Kolakofsky, D. In: Fields Virology, B.N. Fields, D.M. Knipe, P.M. Howley Eds.; Lippincott-Raven: Philadelphia, PA, 2001; pp. 1305-1340.
5. Albertini, A.A.V.; Schoehn, G.; Ruigrok, R.W. Structures impliquées dans la réplication et la transcription des virus à ARN non segmentés de sens négatif. Virologie, 2005, 9, 83-92.
6. Roux, L. Dans le génome des Paramyxovirinae, les promoteurs et leurs activités sont façonnés par la règle de six. Virologie, 2005, 9, 19-34.
7. Horikami, S.M.; Curran, J.; Kolakofsky, D.; Moyer, S.A. Complexes of Sendai virus NP-P and P-L proteins are required for defective interfering particle genome replication in vitro. J. Virol., 1992, 66, 4901-4908.
8. Qanungo, K.R.; Shaji, D.; Mathur, M.; Banerjee, A.K. Two RNA polymerase complexes from vesicular stomatitis virus-infected cells that carry out transcription and replication of genome RNA. Proc. Natl. Acad. Sci. USA, 2004, 101, 5952-5957.
9. Gombart, A.F.; Hirano, A.; Wong, T.C. Conformational maturation of measles virus nucleocapsid protein. J. Virol., 1993, 67, 4133-4141.
10. Horikami, S.M.; Moyer, S.A. Structure, transcription, and replication of measles virus. Curr. Top Microbiol. Immunol., 1995, 191, 35-50.
11. Sato, H.; Masuda, M.; Miura, R.; Yoneda, M.; Kai, C. Morbillivirus nucleoprotein possesses a novel nuclear localization signal and a CRM1-independent nuclear export signal. Virology, 2006, 352, 121-130.
12. Huber, M.; Cattaneo, R.; Spielhofer, P.; Orvell, C.; Norrby, E.; Messerli, M.; Perriard, J.C.; Billeter, M.A. Measles virus phosphoprotein retains the nucleocapsid protein in the cytoplasm. Virology, 1991, 185, 299-308.
13. Spehner, D.; Drillien, R.; Howley, P.M. The assembly of the measles virus nucleoprotein into nucleocapsid-like particles is modulated by the phosphoprotein. Virology, 1997, 232, 260-268.
14. Ryan, K.W.; Portner, A. Separate domains of Sendai virus P protein are required for binding to viral nucleocapsids. Virology, 1990, 174, 515-521.
15. Buchholz, C.J.; Retzler, C.; Homann, H.E.; Neubert, W.J. The carboxy-terminal domain of Sendai virus nucleocapsid protein is involved in complex formation between phosphoprotein and nucleocapsid-like particles. Virology, 1994, 204, 770-776.
16. Ferron, F.; Longhi, S.; Henrissat, B.; Canard, B. Viral RNApolymerases-a predicted 2'-O-ribose methyltransferase domain shared by all Mononegavirales. Trends Biochem. Sci., 2002, 27, 222-224.
17. Ogino, T.; Kobayashi, M.; Iwama, M.; Mizumoto, K. Sendai virus RNA-dependent RNA polymerase L protein catalyzes cap methylation of virus-specific mRNA. J. Biol. Chem., 2005, 280, 4429-4435.
18. Bourhis, J.M.; Canard, B.; Longhi, S. Structural disorder within the replicative complex of measles virus: functional implications. Virology, 2006, 344, 94-110.
19. Bourhis, J.M.; Longhi, S. In: Measles virus nucleoprotein, S. Longhi Ed.; Nova Publishers Inc.: Hauppage, NY, 2007; pp. 1-35.
20. Longhi, S. Nucleocapsid structure and function. Curr. Top Microbiol. Immunol., 2009, 329, 103-128.
21. Schoehn, G.; Iseni, F.; Mavrakis, M.; Blondel, D.; Ruigrok, R.W. Structure of recombinant rabies virus nucleoprotein-RNA complex and identification of the phosphoprotein binding site. J. Virol., 2001, 75, 490-498.
22. Karlin, D.; Longhi, S.; Canard, B. Substitution of two residues in the measles virus nucleoprotein results in an impaired selfassociation. Virology, 2002, 302, 420-432.
23. Karlin, D.; Longhi, S.; Receveur, V.; Canard, B. The N-terminal domain of the phosphoprotein of morbilliviruses belongs to the natively unfolded class of proteins. Virology, 2002, 296, 251-262.
24. Karlin, D.; Ferron, F.; Canard, B.; Longhi, S. Structural disorder and modular organization in Paramyxovirinae N and P. J. Gen. Virol., 2003, 84, 3239-3252.
25. Longhi, S.; Receveur-Brechot, V.; Karlin, D.; Johansson, K.; Darbon, H.; Bhella, D.; Yeo, R.; Finet, S.; Canard, B. 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., 2003, 278, 18638-18648.
26. Bourhis, J.; Johansson, K.; Receveur-Bréchot, V.; Oldfield, C.J.; Dunker, A.K.; Canard, B.; Longhi, S. The C-terminal domain of measles virus nucleoprotein belongs to the classof intrinsically disordered proteins that fold upon binding to their pohysiological partner. Virus Research, 2004, 99, 157-167.
27. Bourhis, J.M.; Receveur-Bréchot, V.; Oglesbee, M.; Zhang, X.; Buccellato, M.; Darbon, H.; Canard, B.; Finet, S.; Longhi, S. 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., 2005, 14, 1975-1992.
28. Bourhis, J.M.; Canard, B.; Longhi, S. Désordre structural au sein du complexe réplicatif du virus de la rougeole: implications fonctionnelles. Virologie, 2005, 9, 367-383.
29. Radivojac, P.; Iakoucheva, L.M.; Oldfield, C.J.; Obradovic, Z.; Uversky, V.N.; Dunker, A.K. Intrinsic disorder and functional proteomics. Biophys J, 2007, 92, 1439-1456.
30. Ferron, F.; Longhi, S.; Canard, B.; Karlin, D. A practical overview of protein disorder prediction methods. Proteins, 2006, 65, 1-14.
31. Bourhis, J.M.; Canard, B. and Longhi, S. Predicting protein disorder and induced folding: from theoretical principles to practical applications. Curr. Protein Pept. Sci., 2007, 8, 135-149.
32. Receveur-Bréchot, V.; Bourhis, J.M.; Uversky, V.N.; Canard, B.; Longhi, S. Assessing protein disorder and induced folding. Proteins: Structure, Function and Bioinformatics, 2006, 62, 24-45.
33. Gerard, F.C.; Ribeiro Ede, A., Jr.; Leyrat, C.; Ivanov, I.; Blondel, D.; Longhi, S.; Ruigrok, R.W. and Jamin, M. Modular organization of rabies virus phosphoprotein. J Mol Biol, 2009, 388, 978-996.
34. Llorente, M.T.; Barreno-Garcia, B.; Calero, M.; Camafeita, E.; Lopez, J.A.; Longhi, S.; Ferron, F.; Varela, P.F.; Melero, J.A. Structural analysis of the human respiratory syncitial virus phosphoprotein: characterization of an a-helical domain involved in oligomerization. J. Gen. Virol., 2006, 87, 159-169.
35. Tarbouriech, N.; Curran, J.; Ebel, C.; Ruigrok, R.W.; Burmeister, W.P. On the domain structure and the polymerization state of the sendai virus P protein. Virology, 2000, 266, 99-109.
36. Tarbouriech, N.; Curran, J.; Ruigrok, R.W.; Burmeister, W.P. Tetrameric coiled coil domain of Sendai virus phosphoprotein. Nat. Struct. Biol., 2000, 7, 777-781.
37. Chen, M.; Cortay, J.C. and Gerlier, D. Measles virus protein interactions in yeast: new findings and caveats. Virus Res, 2003, 98, 123-129.
38. Li, X.; Romero, P.; Rani, M.; Dunker, A.K.; Obradovic, Z. Predicting Protein Disorder for N-, C-, and Internal Regions. Genome Inform. Ser. Workshop Genome Inform., 1999, 10, 30-40.
39. Uversky, V.N.; Gillespie, J.R.; Fink, A.L. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins, 2000, 41, 415-427.
40. Lieutaud, P.; Canard, B.; Longhi, S. MeDor: a metaserver for predicting protein disorder. BMC Genomics, 2008, 9, S25.
41. Melcher, K. The strength of acidic activation domains correlates with their affinity for both transcriptional and non-transcriptional proteins. J. Mol. Biol., 2000, 301, 1097-1112.
42. Curran, J.; Marq, J.B.; Kolakofsky, D. An N-terminal domain of the Sendai paramyxovirus P protein acts as a chaperone for the NP protein during the nascent chain assembly step of genome replication. J. Virol., 1995, 69, 849-855.
43. Sweetman, D.A.; Miskin, J.; Baron, M.D. Rinderpest virus C and V proteins interact with the major (L) component of the viral polymerase. Virology, 2001, 281, 193-204.
44. Smallwood, S.; Ryan, K.W.; Moyer, S.A. Deletion analysis defines a carboxyl-proximal region of Sendai virus P protein that binds to the polymerase L protein. Virology, 1994, 202, 154-163.
45. Chen, M.; Cortay, J.C.; Logan, I.R.; Sapountzi, V.; Robson, C.N.; Gerlier, D. Inhibition of ubiquitination and stabilization of human ubiquitin E3 ligase PIRH2 by measles virus phosphoprotein. J. Virol., 2005, 79, 11824-11836.
46. Johansson, K.; Bourhis, J.M.; Campanacci, V.; Cambillau, C.; Canard, B.; Longhi, S. Crystal structure of the measles virus phosphoprotein domain responsible for the induced folding of the Cterminal domain of the nucleoprotein. J. Biol. Chem., 2003, 278, 44567-44573.
47. Rahaman, A.; Srinivasan, N.; Shamala, N.; Shaila, M.S. Phosphoprotein of the rinderpest virus forms a tetramer through a coiled coil region important for biological function. A structural insight. J. Biol. Chem., 2004, 279, 23606-23614.
48. Kingston, R.L.; Gay, L.S.; Baase, W.S.; Matthews, B.W. Structure of the nucleocapsid-binding domain from the mumps virus polymerase; an example of protein folding induced by crystallization. J. Mol. Biol., 2008, 379, 719-731.
49. Blanchard, L.; Tarbouriech, N.; Blackledge, M.; Timmins, P.; Burmeister, W.P.; Ruigrok, R.W.; Marion, D. Structure and dynamics of the nucleocapsid-binding domain of the Sendai virus phosphoprotein in solution. Virology, 2004, 319, 201-211.
50. Kingston, R.L.; Walter, A.B.; Gay, L.S. Characterization of nucleocapsid binding by the measles and the mumps virus phosphoprotein. J. Virol., 2004, 78, 8615-8629.
51. Bernado, P.; Blanchard, L.; Timmins, P.; Marion, D.; Ruigrok, R.W.; Blackledge, M. A structural model for unfolded proteins from residual dipolar couplings and small-angle x-ray scattering. Proc. Natl. Acad. Sci. USA, 2005, 102, 17002-17007.
52. Houben, K.; Blanchard, L.; Blackledge, M.; Marion, D. Intrinsic dynamics of the partly unstructured PX domain from the Sendai virus RNA polymerase cofactor P. Biophys. J., 2007, 93, 2830-2844.
53. Jordan, I.K.; Sutter, B.A.; McClure, M.A. Molecular evolution of the Paramyxoviridae and Rhabdoviridae multiple-protein-encoding P gene. Mol. Biol. Evol., 2000, 17, 75-86.
54. Narechania, A.; Terai, M.; Burk, R.D. Overlapping reading frames in closely related human papillomaviruses result in modular rates of selection within E2. J. Gen. Virol., 2005, 86, 1307-1313.
55. Rancurel, C.; Khosravi, M.; Dunker, K.A.; Romero, P.R.; Karlin, D. Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J. Virol., 2009, 83(20), 10719-36.
56. Curran, J.; Homann, H.; Buchholz, C.; Rochat, S.; Neubert, W.; Kolakofsky, D. The hypervariable C-terminal tail of the Sendai paramyxovirus nucleocapsid protein is required for template function but not for RNA encapsidation. J. Virol., 1993, 67, 4358-4364.
57. Buchholz, C.J.; Spehner, D.; Drillien, R.; Neubert, W.J.; Homann, H.E. The conserved N-terminal region of Sendai virus nucleocapsid protein NP is required for nucleocapsid assembly. J. Virol., 1993, 67, 5803-5812.
58. Bankamp, B.; Horikami, S.M.; Thompson, P.D.; Huber, M.; Billeter, M.; Moyer, S.A. Domains of the measles virus N protein required for binding to P protein and self-assembly. Virology, 1996, 216, 272-277.
59. Liston, P.; Batal, R.; DiFlumeri, C.; Briedis, D.J. Protein interaction domains of the measles virus nucleocapsid protein (NP). Arch. Virol., 1997, 142, 305-321.
60. Myers, T.M.; Pieters, A.; Moyer, S.A. A highly conserved region of the Sendai virus nucleocapsid protein contributes to the NP-NP binding domain. Virology, 1997, 229, 322-335.
61. Myers, T.M.; Smallwood, S.; Moyer, S.A. Identification of nucleocapsid protein residues required for Sendai virus nucleocapsid formation and genome replication. J. Gen. Virol., 1999, 80, 1383-1391.
62. Heggeness, M.H.; Scheid, A.; Choppin, P.W. Conformation of the helical nucleocapsids of paramyxoviruses and vesicular stomatitis virus: reversible coiling and uncoiling induced by changes in salt concentration. Proc. Natl. Acad. Sci. USA, 1980, 77, 2631-2635.
63. Heggeness, M.H.; Scheid, A.; Choppin, P.W. The relationship of conformational changes in the Sendai virus nucleocapsid to proteolytic cleavage of the NP polypeptide. Virology, 1981, 114, 555-562.
64. Spehner, D.; Kirn, A.; Drillien, R. Assembly of nucleocapsidlike structures in animal cells infected with a vaccinia virus recombinant encoding the measles virus nucleoprotein. J. Virol., 1991, 65, 6296-6300.
65. Warnes, A.; Fooks, A.R.; Dowsett, A.B.; Wilkinson, G.W.; Stephenson, J.R. Expression of the measles virus nucleoprotein gene in Escherichia coli and assembly of nucleocapsid-like structures. Gene, 1995, 160, 173-178.
66. Bhella, D.; Ralph, A.; Murphy, L.B.; Yeo, R.P. Significant differences in nucleocapsid morphology within the Paramyxoviridae. J. Gen. Virol., 2002, 83, 1831-1839.
67. Bhella, D.; Ralph, A.; Yeo, R.P. Conformational flexibility in recombinant measles virus nucleocapsids visualised by cryo-negative stain electron microscopy and real-space helical reconstruction. J. Mol. Biol., 2004, 340, 319-331.
68. Schoehn, G.; Mavrakis, M.; Albertini, A.; Wade, R.; Hoenger, A.; Ruigrok, R.W. The 12 A structure of trypsin-treated measles virus N-RNA. J. Mol. Biol., 2004, 339, 301-312.
69. Egelman, E.H.; Wu, S.S.; Amrein, M.; Portner, A.; Murti, G. The Sendai virus nucleocapsid exists in at least four different helical states. J. Virol., 1989, 63, 2233-2243.
70. Robbins, S.J.; Bussell, R.H.; Rapp, F. Isolation and partial characterization of two forms of cytoplasmic nucleocapsids from measles virus-infected cells. J. Gen. Virol., 1980, 47, 301-310.
71. Green, T.J.; Zhang, X.; Wertz, G.W.; Luo, M. Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science, 2006, 313, 357-360.
72. Albertini, A.A.; Wernimont, A.K.; Muziol, T.; Ravelli, R.B.; Clapier, C.R.; Schoehn, G.; Weissenhorn, W.; Ruigrok, R.W. Crystal structure of the rabies virus nucleoprotein-RNA complex. Science, 2006, 313, 360-363.
73. Luo, M.; Green, T.J.; Zhang, X.; Tsao, J. and Qiu, S. Conserved characteristics of the rhabdovirus nucleoprotein. Virus Res., 2007, 129, 246-251.
74. Tawar, R.G.; Duquerroy, S.; Vonrhein, C.; Varela, P.F.; Damier-Piolle, L.; Castagné, N.; MacLellan, K.; Bedouelle, H.; Bricogne, G.; Bhella, D.; Eleouet, J.F.; Rey, F.A. 3D structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science, 2009, 326, 1279-1283.
75. Rudolph, M.G.; Kraus, I.; Dickmanns, A.; Eickmann, M.; Garten, W.; Ficner, R. Crystal structure of the borna disease virus nucleoprotein. Structure (Camb), 2003, 11, 1219-1226.
76. Kouznetzoff, A.; Buckle, M.; Tordo, N. Identification of a region of the rabies virus N protein involved in direct binding to the viral RNA. J. Gen. Virol., 1998, 79, 1005-1013.
77. Giraudon, P.; Jacquier, M.F.; Wild, T.F. Antigenic analysis of African measles virus field isolates: identification and localisation of one conserved and two variable epitope sites on the NP protein. Virus Res., 1988, 10, 137-152.
78. Baker, S.C.; Moyer, S.A. Encapsidation of Sendai virus genome RNAs by purified NP protein during in vitro replication. J. Virol., 1988, 62, 834-838.
79. Dunker, A.K.; Lawson, J.D.; Brown, C.J.; Williams, R.M.; Romero, P.; Oh, J.S.; Oldfield, C.J.; Campen, A.M.; Ratliff, C.M.; Hipps, K.W.; Ausio, J.; Nissen, M.S.; Reeves, R.; Kang, C.; Kissinger, C.R.; Bailey, R.W.; Griswold, M.D.; Chiu, W.; Garner, E.C.; Obradovic, Z. Intrinsically disordered protein. J. Mol. Graph. Model., 2001, 19, 26-59.
80. Uversky, V.N. Natively unfolded proteins: a point where biology waits for physics. Protein Sci., 2002, 11, 739-756.
81. Tompa, P. Intrinsically unstructured proteins. Trends Biochem. Sci., 2002, 27, 527-533.
82. Fuxreiter, M.; Simon, I.; Friedrich, P.; Tompa, P. Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J. Mol. Biol., 2004, 338, 1015-1026.
83. Lacy, E.R.; Filippov, I.; Lewis, W.S.; Otieno, S.; Xiao, L.; Weiss, S.; Hengst, L.; Kriwacki, R.W. p27 binds cyclin-CDK complexes through a sequential mechanism involving binding-induced protein folding. Nat. Struct. Mol. Biol., 2004, 11, 358-364.
84. Diallo, A.; Barrett, T.; Barbron, M.; Meyer, G.; Lefevre, P.C. Cloning of the nucleocapsid protein gene of peste-des-petits-ruminants virus: relationship to other morbilliviruses. J. Gen. Virol., 1994, 75 (Pt 1), 233-237.
85. Garner, E.; Romero, P.; Dunker, A.K.; Brown, C.; Obradovic, Z. Predicting Binding Regions within Disordered Proteins. Genome Inform. Ser. Workshop Genome Inform., 1999, 10, 41-50.
86. Oldfield, C.J.; Cheng, Y.; Cortese, M.S.; Romero, P.; Uversky, V.N.; Dunker, A.K. Coupled Folding and Binding with alpha-Helix-Forming Molecular Recognition Elements. Biochemistry, 2005, 44, 12454-12470.
87. Mohan, A.; Oldfield, C.J.; Radivojac, P.; Vacic, V.; Cortese, M.S.; Dunker, A.K.; Uversky, V.N. Analysis of Molecular Recognition Features (MoRFs). J. Mol. Biol., 2006, 362, 1043-1059.
88. Vacic, V.; Oldfield, C.J.; Mohan, A.; Radivojac, P.; Cortese, M.S.; Uversky, V.N.; Dunker, A.K. Characterization of molecular recognition features, MoRFs, and their binding partners. J. Proteome Res., 2007, 6, 2351-2366.
89. Kingston, R.L.; Hamel, D.J.; Gay, L.S.; Dahlquist, F.W.; Matthews, B.W. Structural basis for the attachment of a paramyxoviral polymerase to its template. Proc. Natl. Acad. Sci. USA, 2004, 101, 8301-8306.
90. Gely, S.; Lowry, D.F.; Bernard, C.; Ringkjobing-Jensen, M.; Blackledge, M.; Costanzo, S.; Darbon, H.; Daughdrill, G.W.; Longhi, S. 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 J. Mol. Recognit., 2010, in press.
91. Bernard, C.; Gely, S.; Bourhis, J.M.; Morelli, X.; Longhi, S.; Darbon, H. Interaction between the C-terminal domains of N and P proteins of measles virus investigated by NMR. FEBS Lett., 2009, 583, 1084-1089.
92. Houben, K.; Marion, D.; Tarbouriech, N.; Ruigrok, R.W.; Blanchard, L. Interaction of the C-terminal domains of sendai virus N and P proteins: comparison of polymerase-nucleocapsid interactions within the paramyxovirus family. J. Virol., 2007, 81, 6807-6816.
93. Feix, J.B.; Klug, C.S. In: In Biological magnetic resonance, L. Berliner Ed.; Plenum Press: New York, 1998; pp. 251-281.
94. Hubbell, W.L.; Gross, A.; Langen, R.; Lietzow, M.A. Recent advances in site-directed spin labeling of proteins. Curr. Opin. Struct. Biol., 1998, 8, 649-656.
95. Biswas, R.; Kuhne, H.; Brudvig, G.W.; Gopalan, V. Use of EPR spectroscopy to study macromolecular structure and function. Sci. Prog., 2001, 84, 45-67.
96. Morin, B.; Bourhis, J.M.; Belle, V.; Woudstra, M.; Carrière, F.; BGuigliarelli, B.; Fournel, A.; Longhi, S. Assessing induced folding of an intrinsically disordered protein by site-directed spinlabeling EPR spectroscopy. J. Phys. Chem. B, 2006, 110, 20596-20608.
97. Belle, V.; Rouger, S.; Costanzo, S.; Liquiere, E.; Strancar, J.; Guigliarelli, B.; Fournel, A.; Longhi, S. 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 Struct. Funct. Bioinform., 2008, 73, 973-988.
98. Kavalenka, A.; Urbancic, I.; Belle, V.; Rouger, S.; Costanzo, S.; Kure, S.; Fournel, A.; Longhi, S.; Guigliarelli, B.; Strancar, J. Conformational analysis of the partially disordered measles virus NTAIL-XD complex by SDSL EPR spectroscopy. Biophys. J., 2010, 98, 1055-1064.
99. Sivakolundu, S.G.; Bashford, D.; Kriwacki, R.W. Disordered p27Kip1 exhibits intrinsic structure resembling the Cdk2/cyclin Abound conformation. J. Mol. Biol., 2005, 353, 1118-1128.
100. Tsai, C.D.; Ma, B.; Kumar, S.; Wolfson, H.; Nussinov, R. Protein folding: binding of conformationally fluctuating building blocks via population selection. Crit. Rev. Biochem. Mol. Biol., 2001, 36, 399-433.
101. Tsai, C.J.; Ma, B.; Sham, Y.Y.; Kumar, S.; Nussinov, R. Structured disorder and conformational selection. Proteins: Structure, Function and Bioinformatics, 2001, 44, 418-427.
102. Shoemaker, B.A.; Portman, J.J.; Wolynes, P.G. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc. Natl. Acad. Sci. USA, 2000, 97, 8868-8873.
103. Tompa, P.; Fuxreiter, M. Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem. Sci., 2008, 33, 2-8.
104. Oglesbee, M.; Tatalick, L.; Rice, J.; Krakowka, S. Isolation and characterization of canine distemper virus nucleocapsid variants. J. Gen. Virol., 1989, 70 (Pt 9), 2409-2419.
105. Robbins, S.J.; Bussell, R.H. Structural phosphoproteins associated with purified measles virions and cytoplasmic nucleocapsids. Intervirology, 1979, 12, 96-102.
106. Stallcup, K.C.; Wechsler, S.L. and Fields, B.N. Purification of measles virus and characterization of subviral components. J. Virol., 1979, 30, 166-176.
107. Zhang, X.; Glendening, C.; Linke, H.; Parks, C.L.; Brooks, C.; Udem, S.A.; Oglesbee, M. Identification and characterization of a regulatory domain on the carboxyl terminus of the measles virus nucleocapsid protein. J. Virol., 2002, 76, 8737-8746.
108. Vincent, S.; Tigaud, I.; Schneider, H.; Buchholz, C.J.; Yanagi, Y.; Gerlier, D. Restriction of measles virus RNA synthesis by a mouse host cell line: trans-complementation by polymerase components or a human cellular factor(s). J. Virol., 2002, 76, 6121-6130.
109. Fearns, R.; Collins, P.L. Role of the M2-1 transcription antitermination protein of respiratory syncytial virus in sequential transcription. J. Virol., 1999, 73, 5852-5864.
110. Hartlieb, B.; Modrof, J.; Muhlberger, E.; Klenk, H.D.; Becker, S. Oligomerization of Ebola virus VP30 is essential for viral transcription and can be inhibited by a synthetic peptide. J. Biol. Chem., 2003, 278, 41830-41836.
111. Vasconcelos, D.; Norrby, E.; Oglesbee, M. The cellular stress response increases measles virus-induced cytopathic effect. J. Gen. Virol., 1998, 79, 1769-1773.
112. Vasconcelos, D.Y.; Cai, X.H. and Oglesbee, M.J. Constitutive overexpression of the major inducible 70 kDa heat shock protein mediates large plaque formation by measles virus. J. Gen. Virol., 1998, 79, 2239-2247.
113. Oglesbee, M.J.; Kenney, H.; Kenney, T.; Krakowka, S. Enhanced production of morbillivirus gene-specific RNAs following induction of the cellular stress response in stable persistent infection. Virology, 1993, 192, 556-567.
114. Oglesbee, M.J.; Liu, Z.; Kenney, H.; Brooks, C.L. The highly inducible member of the 70 kDa family of heat shock proteins increases canine distemper virus polymerase activity. J. Gen. Virol., 1996, 77, 2125-2135.
115. Zhang, X.; Bourhis, J.M.; Longhi, S.; Carsillo, T.; Buccellato, M.; Morin, B.; Canard, B.; Oglesbee, M. Hsp72 recognizes a P binding motif in the measles virus N protein C-terminus. Virology, 2005, 337, 162-174.
116. Carsillo, T.; Zhang, X.; Vasconcelos, D.; Niewiesk, S.; Oglesbee, M. A single codon in the nucleocapsid protein C terminus contributes to in vitro and in vivo fitness of Edmonston measles virus. J. Virol., 2006, 80, 2904-2912.
117. Oglesbee, M. In: Measles virus nucleoprotein, S. Longhi Ed.; Nova Publishers Inc.: Hauppage, NY, 2007; pp. 53-98.
118. Tapparel, C.; Maurice, D.; Roux, L. The activity of Sendai virus genomic and antigenomic promoters requires a second element past the leader template regions: a motif (GNNNNN)3 is essential for replication. J. Virol., 1998, 72, 3117-3128.
119. Oglesbee, M.; Ringler, S.; Krakowka, S. Interaction of canine distemper virus nucleocapsid variants with 70K heat-shock proteins. J. Gen. Virol., 1990, 71, 1585-1590.
120. Marion, D.; Tarbouriech, N.; Ruigrok, R.W.; Burmeister, W.P.; Blanchard, L. Assignment of the 1H, 15N and 13C resonances of the nucleocapsid-binding domain of the Sendai virus phosphoprotein. J. Biomol. NMR, 2001, 21, 75-76.
121. Cortese, M.S.; Uversky, V.N.; Dunker, A.K. Intrinsic disorder in scaffold proteins: getting more from less. Prog. Biophys. Mol. Biol., 2008, 98, 85-106.
122. Balazs, A.; Csizmok, V.; Buday, L.; Rakacs, M.; Kiss, R.; Bokor, M.; Udupa, R.; Tompa, K.; Tompa, P. High levels of structural disorder in scaffold proteins as exemplified by a novel neuronal protein, CASK-interactive protein1. FEBS J., 2009, 276, 3744-3756.
123. Curran, J.; Pelet, T.; Kolakofsky, D. An acidic activation-like domain of the Sendai virus P protein is required for RNA synthesis and encapsidation. Virology, 1994, 202, 875-884.
124. Harty, R.N.; Palese, P. Measles virus phosphoprotein (P) requires the NH2-and COOH-terminal domains for interactions with the nucleoprotein (N) but only the COOH terminus for interactions with itself. J. Gen. Virol., 1995, 76, 2863-2867.
125. Curran, J.A.; Kolakofsky, D. Rescue of a Sendai virus DI genome by other parainfluenza viruses: implications for genome replication. Virology, 1991, 182, 168-176.
126. Gupta, A.K.; Shaji, D.; Banerjee, A.K. Identification of a novel tripartite complex involved in replication of vesicular stomatitis virus genome RNA. J. Virol., 2003, 77, 732-738.
127. Dunker, A.K.; Cortese, M.S.; Romero, P.; Iakoucheva, L.M.; Uversky, V.N. Flexible nets. FEBS J., 2005, 272, 5129-5148.
128. Uversky, V.N.; Oldfield, C.J.; Dunker, A.K. Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling. J. Mol. Recognit., 2005, 18, 343-384.
129. Haynes, C.; Oldfield, C.J.; Ji, F.; Klitgord, N.; Cusick, M.E.; Radivojac, P.; Uversky, V.N.; Vidal, M.; Iakoucheva, L.M. Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput. Biol., 2006, 2, e100.
130. Tompa, P. The functional benefits of disorder. J. Mol. Struct. (Theochem), 2003, 666-67, 361-371.
131. Dunker, A.K.; Garner, E.; Guilliot, S.; Romero, P.; Albrecht, K.; Hart, J.; Obradovic, Z.; Kissinger, C.; Villafranca, J.E. Protein disorder and the evolution of molecular recognition: theory, predictions and observations. Pac. Symp. Biocomput., 1998, 3, 473-484.
132. Wright, P.E. and Dyson, H.J. Intrinsically unstructured proteins: reassessing the protein structure-function paradigm. J. Mol. Biol., 1999, 293, 321-331.
133. Dunker, A.K.; Obradovic, Z. The protein trinity--linking function and disorder. Nat. Biotechnol., 2001, 19, 805-806.
134. Dunker, A.K.; Brown, C.J.; Obradovic, Z. Identification and functions of usefully disordered proteins. Adv. Protein Chem., 2002, 62, 25-49.
135. Uversky, V.N.; Li, J.; Souillac, P.; Jakes, R.; Goedert, M.; Fink, A.L. Biophysical properties of the synucleins and their propensities to fibrillate: inhibition of alpha-synuclein assembly by beta-and gamma-synucleins. J. Biol. Chem., 2002, 25, 25.
136. Gunasekaran, K.; Tsai, C.J.; Kumar, S.; Zanuy, D.; Nussinov, R. Extended disordered proteins: targeting function with less scaffold. Trends Biochem. Sci., 2003, 28, 81-85.
137. Fink, A.L. Natively unfolded proteins. Curr Opin Struct Biol, 2005, 15, 35-41.
138. Dyson, H.J.; Wright, P.E. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol., 2005, 6, 197-208.
139. Iwasaki, M.; Takeda, M.; Shirogane, Y.; Nakatsu, Y.; Nakamura, T.; Yanagi, Y. The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J. Virol., 2009, 83(20), 10374-83.
140. tenOever, B.R.; Servant, M.J.; Grandvaux, N.; Lin, R.; Hiscott, J. Recognition of the Measles Virus Nucleocapsid as a Mechanism of IRF-3 Activation. J. Virol., 2002, 76, 3659-3669.
141. Colombo, M.; Bourhis, J.M.; Chamontin, C.; Soriano, C.; Villet, S.; Costanzo, S.; Couturier, M.; Belle, V.; Fournel, A.; Darbon, H.; Gerlier, D.; Longhi, S. The interaction between the measles virus nucleoprotein and the Interferon Regulator Factor 3 relies on a specific cellular environment. Virol. J, 2009, 6, 59.
142. De, B.P.; Banerjee, A.K. Involvement of actin microfilaments in the transcription/replication of human parainfluenza virus type 3: possible role of actin in other viruses. Microsc. Res. Tech., 1999, 47, 114-123.
143. Moyer, S.A.; Baker, S.C.; Horikami, S.M. Host cell proteins required for measles virus reproduction. J. Gen. Virol., 1990, 71, 775-783.
144. Marie, J.C.; Kehren, J.; Trescol-Biemont, M.C.; Evlashev, A.; Valentin, H.; Walzer, T.; Tedone, R.; Loveland, B.; Nicolas, J.F.; Rabourdin-Combe, C.; Horvat, B. Mechanism of measles virusinduced suppression of inflammatory immune responses. Immunity, 2001, 14, 69-79.
145. Laine, D.; Trescol-Biémont, M.; Longhi, S.; Libeau, G.; Marie, J.; Vidalain, P.; Azocar, O.; Diallo, A.; Canard, B.; Rabourdin-Combe, C.; Valentin, H. Measles virus nucleoprotein binds to a novel cell surface receptor distinct from FcgRII via its C-terminal domain: role in MV-induced immunosuppression. J. Virol., 2003, 77, 11332-11346.
146. Laine, D.; Bourhis, J.; Longhi, S.; Flacher, M.; Cassard, L.; Canard, B.; Sautès-Fridman, C.; Rabourdin-Combe, C.; Valentin, H. Measles virus nucleoprotein induces cell proliferation arrest and apoptosis through NTAIL/NR and NCORE/FcgRIIB1 interactions, respectively. J. Gen. Virol., 2005, 86, 1771-1784.
147. Liston, P.; DiFlumeri, C.; Briedis, D.J. Protein interactions entered into by the measles virus P, V, and C proteins. Virus Res., 1995, 38, 241-259.
148. Oglesbee, M.J.; Pratt, M.; Carsillo, T. Role for heat shock proteins in the immune response to measles virus infection. Viral Immunol., 2002, 15, 399-416.
149. Carsillo, T.; Carsillo, M.; Niewiesk, S.; Vasconcelos, D.; Oglesbee, M. Hyperthermic pre-conditioning promotes measles virus clearance from brain in a mouse model of persistent infection. Brain Res., 2004, 1004, 73-82.
150. Carsillo, T.; Carsillo, M.; Traylor, Z.; Rajala-Schultz, P.; Popovich, P.; Niewiesk, S.; Oglesbee, M. Major histocompatibility complex haplotype determines hsp70-dependent protection against measles virus neurovirulence. J. Virol., 2009, 83, 5544-5555.
151. Carsillo, T.; Traylor, Z.; Choi, C.; Niewiesk, S.; Oglesbee, M. hsp72, a host determinant of measles virus neurovirulence. J. Virol., 2006, 80, 11031-11039.
152. Couturier, M.; Buccellato, M.; Costanzo, S.; Bourhis, J.M.; Shu, Y.; Nicaise, M.; Desmadril, M.; Flaudrops, C.; Longhi, S. Oglesbee, M. High Affinity Binding between Hsp70 and the C-Terminal Domain of the Measles Virus Nucleoprotein Requires an Hsp40 Co-Chaperone. J. Mol. Recognit., 2009, in press.
153. Cheng, Y.; Legall, T.; Oldfield, C.J.; Mueller, J.P.; Van, Y.Y.; Romero, P.; Cortese, M.S.; Uversky, V.N. and Dunker, A.K. Rational drug design via intrinsically disordered protein. Trends Biotechnol, 2006, 24, 435-442.
154. Chinchar, V.G.; Portner, A. Functions of Sendai virus nucleocapsid polypeptides: enzymatic activities in nucleocapsids following cleavage of polypeptide P by Staphylococcus aureus protease V8. Virology, 1981, 109, 59-71.
155. Deshpande, K.L.; Portner, A. Monoclonal antibodies to the P protein of Sendai virus define its structure and role in transcription. Virology, 1985, 140, 125-134.
156. Dedmon, M.M.; Patel, C.N.; Young, G.B.; Pielak, G.J. FlgM gains structure in living cells. Proc. Natl. Acad. Sci. USA, 2002, 99, 12681-12684.
157. McNulty, B.C.; Young, G.B.; Pielak, G.J. Macromolecular crowding in the Escherichia coli periplasm maintains alpha-synuclein disorder. J. Mol. Biol., 2006, 355, 893-897.
158. Bodart, J.F.; Wieruszeski, J.M.; Amniai, L.; Leroy, A.; Landrieu, I.; Rousseau-Lescuyer, A.; Vilain, J.P. and Lippens, G. NMR observation of Tau in Xenopus oocytes. J. Magn. Reson., 2008, 192, 252-257.
159. Chen, J.W.; Romero, P.; Uversky, V.N.; Dunker, A.K. Conservation of intrinsic disorder in protein domains and families: I. A database of conserved predicted disordered regions. J. Proteome Res., 2006, 5, 879-887.
160. Tokuriki, N.; Oldfield, C.J.; Uversky, V.N.; Berezovsky, I.N.; Tawfik, D.S. Do viral proteins possess unique biophysical features? Trends Biochem. Sci, 2009, 34, 53-59.
161. Curran, J. and Kolakofsky, D. Replication of paramyxoviruses. Adv. Virus Res., 1999, 54, 403-422.
162. DeLano, W.L. The PyMOL molecular graphics system Proteins: Structure, Function and Bioinformatics, 2002, 30, 442-454.