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Fuzziness pp 126-141 | Cite as

The Measles Virus NTAIL-XD Complex: An Illustrative Example of Fuzziness

  • Sonia Longhi
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 725)

Abstract

In this chapter, I focus on the biochemical and structural characterization of the complex between the intrinsically disordered C-terminal domain of the measles virus nucleoprotein (NTAIL) and the C-terminal X domain (XD) of the viral phosphoprotein (P). I summarize the main experimental data available so far pointing out the prevalently disordered nature of NTAIL even after complex formation and the role of the flexible C-terminal appendage in the binding reaction. I finally discuss the possible functional role of these residual disordered regions within the complex in terms of their ability to capture other regulatory, binding partners.

Keywords

Canine Distemper Virus Virus Polymerase Activity Viral Phosphoprotein Measle Virus Nucleoprotein Gulatory Role 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Longhi S, Canard B. Mécanismes de transcription et de réplication des Paramyxoviridae. Virologie 1999; 3:227–240.Google Scholar
  2. 2.
    Lamb RA, Kolakofsky D. Paramyxoviridae: the viruses and their replication. In: Fields BN, Knipe DM, Howley PM, eds. Fields Virology. 4th ed. Philadelphia, PA: Lippincott-Raven 2001:1305–1340.Google Scholar
  3. 3.
    Albertini AAV, Schoehn G, Ruigrok RW. Structures impliquées dans la réplication et la transcription des virus à ARN non segmentés de sens négatif. Virologie 2005; 9:83–92.Google Scholar
  4. 4.
    Roux L. Dans le génome des Paramyxovirinae, les promoteurs et leurs activités sont façonnés par la « règle de six. Virologie 2005; 9:19–34.Google Scholar
  5. 5.
    Karlin D, Longhi S, Receveur V et al. The N-terminal domain of the phosphoprotein of morbilliviruses belongs to the natively unfolded class of proteins. Virology 2002; 296:251–262.PubMedCrossRefGoogle Scholar
  6. 6.
    Longhi S, Receveur-Brechot V, Karlin D et al. 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.PubMedCrossRefGoogle Scholar
  7. 7.
    Karlin D, Ferron F, Canard B et al. Structural disorder and modular organization in Paramyxovirinae N and P. J Gen Virol 2003; 84:3239–3252.PubMedCrossRefGoogle Scholar
  8. 8.
    Bourhis J, Johansson K, Receveur-Bréchot V et al. The C-terminal domain of measles virus nucleoprotein belongs to the class of intrinsically disordered proteins that fold upon binding to their pohysiological partner. Virus Research 2004; 99:157–167.PubMedCrossRefGoogle Scholar
  9. 9.
    Bourhis JM, Receveur-Bréchot V, Oglesbee M et al. 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.PubMedCrossRefGoogle Scholar
  10. 10.
    Bourhis JM, Canard B, Longhi S. Désordre structural au sein du complexe réplicatif du virus de la rougeole: implications fonctionnelles. Virologie 2005; 9:367–383.Google Scholar
  11. 11.
    Bourhis JM, Canard B, Longhi S. Structural disorder within the replicative complex of measles virus: functional implications. Virology 2006; 344:94–110.PubMedCrossRefGoogle Scholar
  12. 12.
    Bourhis JM, Longhi S. Measles virus nucleoprotein: structural organization and functional role of the intrinsically disordered C-terminal domain. In: Longhi S, ed. Measles virus nucleoprotein. Hauppage, NY: Nova Publishers Inc., 2007:1–35.Google Scholar
  13. 13.
    Longhi S. Nucleocapsid Structure and Function. Curr Top Microbiol Immunol 2009; 329:103–128.PubMedCrossRefGoogle Scholar
  14. 14.
    Longhi S, Oglesbee M. Structural disorder within the measles virus nucleoprotein and phosphoprotein. Protein and Peptide Letters 2010; 17:961–978.PubMedCrossRefGoogle Scholar
  15. 15.
    Radivojac P, Iakoucheva LM, Oldfield CJ et al. Intrinsic disorder and functional proteomics. Biophys J 2007; 92:1439–1456.PubMedCrossRefGoogle Scholar
  16. 16.
    Dunker AK, Oldfield CJ, Meng J et al. The unfoldomics decade: an update on intrinsically disordered proteins. BMC Genomics 2008; 9 Suppl 2:S1.CrossRefGoogle Scholar
  17. 17.
    Dunker AK, Silman I, Uversky VN et al. Function and structure of inherently disordered proteins. Curr Opin Struct Biol 2008; 18:756–764.PubMedCrossRefGoogle Scholar
  18. 18.
    Uversky VN. The mysterious unfoldome: structureless, underappreciated, yet vital part of any given proteome. J Biomed Biotechnol 2010; 2010:568068.PubMedCrossRefGoogle Scholar
  19. 19.
    Karlin D, Longhi S, Canard B. Substitution of two residues in the measles virus nucleoprotein results in an impaired self-association. Virology 2002; 302:420–432.PubMedCrossRefGoogle Scholar
  20. 20.
    Dunker AK, Cortese MS, Romero P et al. Flexible nets. Febs J 2005; 272:5129–5148.PubMedCrossRefGoogle Scholar
  21. 21.
    Uversky VN, Oldfield CJ, Dunker AK. Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling. J Mol Recognit 2005; 18:343–384.PubMedCrossRefGoogle Scholar
  22. 22.
    Haynes C, Oldfield CJ, Ji F et al. Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput Biol 2006; 2:e100.PubMedCrossRefGoogle Scholar
  23. 23.
    Liston P, Batal R, DiFlumeri C et al. Protein interaction domains of the measles virus nucleocapsid protein (NP). Arch Virol 1997; 142:305–321.PubMedCrossRefGoogle Scholar
  24. 24.
    Bankamp B, Horikami SM, Thompson PD et al. Domains of the measles virus N protein required for binding to P protein and self-assembly. Virology 1996; 216:272–277.PubMedCrossRefGoogle Scholar
  25. 25.
    Kingston RL, Walter AB, Gay LS. Characterization of nucleocapsid binding by the measles and the mumps virus phosphoprotein. J Virol 2004; 78:8615–8629.CrossRefGoogle Scholar
  26. 26.
    Iwasaki M, Takeda M, Shirogane Y et al. The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J Virol 2009.Google Scholar
  27. 27.
    Zhang X, Glendening C, Linke H et al. Identification and characterization of a regulatory domain on the carboxyl terminus of the measles virus nucleocapsid protein. J Virol 2002; 76:8737–8746.PubMedCrossRefGoogle Scholar
  28. 28.
    Zhang X, Bourhis JM, Longhi S et al. Hsp72 recognizes a P binding motif in the measles virus N protein C-terminus. Virology 2005; 337:162–174.PubMedCrossRefGoogle Scholar
  29. 29.
    tenOever BR, Servant MJ, Grandvaux N et al. Recognition of the Measles Virus Nucleocapsid as a Mechanism of IRF-3 Activation. J Virol 2002; 76:3659–3669.PubMedCrossRefGoogle Scholar
  30. 30.
    Colombo M, Bourhis JM, Chamontin C et al. The interaction between the measles virus nucleoprotein and the Interferon Regulator Factor 3 relies on a specific cellular environment. Virol J 2009; 6:59.PubMedCrossRefGoogle Scholar
  31. 31.
    Sato H, Masuda M, Miura R et al. Morbillivirus nucleoprotein possesses a novel nuclear localization signal and a CRM1-independent nuclear export signal. Virology 2006; 352:121–130.PubMedCrossRefGoogle Scholar
  32. 32.
    Marie JC, Kehren J, Trescol-Biemont MC et al. Mechanism of measles virus-induced suppression of inflammatory immune responses. Immunity 2001; 14:69–79.PubMedCrossRefGoogle Scholar
  33. 33.
    Laine D, Trescol-Biémont M, Longhi S et al. 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.PubMedCrossRefGoogle Scholar
  34. 34.
    Laine D, Bourhis J, Longhi S et al. Measles virus nucleoprotein induces cell proliferation arrest and apoptosis through NTAIL/NR and NCORE/FcgRIIB1 interactions, respectively. J Gen Virol 2005; 86:1771–1784.PubMedCrossRefGoogle Scholar
  35. 35.
    Laine D, Vidalain P, Gahnnam A et al. Interaction of measles virus nucleoprotein with cell surface receptors: impact on cell biology and immune response. In: Longhi S, ed. Measles virus nucleoprotein. Hauppage, NY: Nova Publishers Inc., 2007:113–152.Google Scholar
  36. 36.
    Chen M, Cortay JC, Gerlier D. Measles virus protein interactions in yeast: new findings and caveats. Virus Res 2003; 98:123–129.PubMedCrossRefGoogle Scholar
  37. 37.
    Liston P, DiFlumeri C, Briedis DJ. Protein interactions entered into by the measles virus P, V and C proteins. Virus Res 1995; 38:241–259.PubMedCrossRefGoogle Scholar
  38. 38.
    Uversky VN. Natively unfolded proteins: a point where biology waits for physics. Protein Sci 2002; 11:739–756.PubMedCrossRefGoogle Scholar
  39. 39.
    Dunker AK, Lawson JD, Brown CJ et al. Intrinsically disordered protein. J Mol Graph Model 2001; 19:26–59.PubMedCrossRefGoogle Scholar
  40. 40.
    Tompa P. Intrinsically unstructured proteins. Trends Biochem Sci 2002; 27:527–533.PubMedCrossRefGoogle Scholar
  41. 41.
    Fuxreiter M, Simon I, Friedrich P et al. Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J Mol Biol 2004; 338:1015–1026.PubMedCrossRefGoogle Scholar
  42. 42.
    Lacy ER, Filippov I, Lewis WS et al. P27 binds cyclin-CDK complexes through a sequential mechanism involving binding-induced protein folding. Nat Struct Mol Biol 2004; 11:358–364.PubMedCrossRefGoogle Scholar
  43. 43.
    Diallo A, Barrett T, Barbron M et al. 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.PubMedCrossRefGoogle Scholar
  44. 44.
    Garner E, Romero P, Dunker AK et al. Predicting Binding Regions within Disordered Proteins. Genome Inform Ser Workshop Genome Inform 1999; 10:41–50.PubMedGoogle Scholar
  45. 45.
    Oldfield CJ, Cheng Y, Cortese MS et al. Coupled Folding and Binding with alpha-Helix-Forming Molecular Recognition Elements. Biochemistry 2005; 44:12454–12470.PubMedCrossRefGoogle Scholar
  46. 46.
    Mohan A, Oldfield CJ, Radivojac P et al. Analysis of Molecular Recognition Features (MoRFs). J Mol Biol 2006; 362:1043–1059.PubMedCrossRefGoogle Scholar
  47. 47.
    Vacic V, Oldfield CJ, Mohan A et al. Characterization of molecular recognition features, MoRFs and their binding partners. J Proteome Res 2007; 6:2351–2366.PubMedCrossRefGoogle Scholar
  48. 48.
    Johansson K, Bourhis JM, Campanacci V et al. Crystal structure of the measles virus phosphoprotein domain responsible for the induced folding of the C-terminal domain of the nucleoprotein. J Biol Chem 2003; 278:44567–44573.PubMedCrossRefGoogle Scholar
  49. 49.
    Kingston RL, Hamel DJ, Gay LS et al. Structural basis for the attachment of a paramyxoviral polymerase to its template. Proc Natl Acad Sci USA 2004; 101:8301–8306.PubMedCrossRefGoogle Scholar
  50. 50.
    Meszaros B, Tompa P, Simon I et al. Molecular principles of the interactions of disordered proteins. J Mol Biol 2007; 372:549–561.PubMedCrossRefGoogle Scholar
  51. 51.
    Tompa P, Fuxreiter M. Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem Sci 2008; 33:2–8.PubMedCrossRefGoogle Scholar
  52. 52.
    Gely S, Lowry DF, Bernard C et al. 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; 23:435–447.PubMedCrossRefGoogle Scholar
  53. 53.
    Bernard C, Gely S, Bourhis JM et al. Interaction between the C-terminal domains of N and P proteins of measles virus investigated by NMR. FEBS Lett 2009; 583:1084–1089.PubMedCrossRefGoogle Scholar
  54. 54.
    Belle V, Rouger S, Costanzo S et al. Site-directed spin labeling EPR spectroscopy. In: Uversky VN, Longhi S, eds. Instrumental analysis of intrinsically disordered proteins: assessing structure and conformation. Hoboken, New Jersey John Wiley and Sons, 2010.Google Scholar
  55. 55.
    Morin B, Bourhis JM, Belle V et al. Assessing induced folding of an intrinsically disordered protein by site-directed spin-labeling EPR spectroscopy. J Phys Chem B 2006; 110:20596–20608.PubMedCrossRefGoogle Scholar
  56. 56.
    Belle V, Rouger S, Costanzo S et al. 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 2008; 73:973–988.CrossRefGoogle Scholar
  57. 57.
    Kavalenka A, Urbancic I, Belle V et al. Conformational analysis of the partially disordered measles virus NTAIL-XD complex by SDSL EPR spectroscopy. Biophys J 2010; 98:1055–1064.PubMedCrossRefGoogle Scholar
  58. 58.
    Tompa P. The functional benefits of disorder. J Mol Structure (Theochem) 2003; 666–667:361–371.CrossRefGoogle Scholar
  59. 59.
    Dunker AK, Garner E, Guilliot S et al. Protein disorder and the evolution of molecular recognition: theory, predictions and observations. Pac Symp Biocomput 1998; 3:473–484.Google Scholar
  60. 60.
    Wright PE, Dyson HJ. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 1999; 293:321–331.PubMedCrossRefGoogle Scholar
  61. 61.
    Dunker AK, Obradovic Z. The protein trinity—linking function and disorder. Nat Biotechnol 2001; 19:805–806.PubMedCrossRefGoogle Scholar
  62. 62.
    Dunker AK, Brown CJ, Obradovic Z. Identification and functions of usefully disordered proteins. Adv Protein Chem 2002; 62:25–49.PubMedCrossRefGoogle Scholar
  63. 63.
    Uversky VN, Li J, Souillac P et al. 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.Google Scholar
  64. 64.
    Gunasekaran K, Tsai CJ, Kumar S et al. Extended disordered proteins: targeting function with less scaffold. Trends Biochem Sci 2003; 28:81–85.PubMedCrossRefGoogle Scholar
  65. 65.
    Fink AL. Natively unfolded proteins. Curr Opin Struct Biol 2005; 15:35–41.PubMedCrossRefGoogle Scholar
  66. 66.
    Dyson HJ, Wright PE. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 2005; 6:197–208.PubMedCrossRefGoogle Scholar
  67. 67.
    Sivakolundu SG, Bashford D, Kriwacki RW. Disordered p27Kip1 exhibits intrinsic structure resembling the Cdk2/cyclin A-bound conformation. J Mol Biol 2005; 353:1118–1128.PubMedCrossRefGoogle Scholar
  68. 68.
    Plumet S, Duprex WP, Gerlier D. Dynamics of viral RNA synthesis during measles virus infection. J Virol 2005; 79:6900–6908.PubMedCrossRefGoogle Scholar
  69. 69.
    Oglesbee M, Tatalick L, Rice J et al. Isolation and characterization of canine distemper virus nucleocapsid variants. J Gen Virol 1989; 70(Pt 9):2409–2419.PubMedCrossRefGoogle Scholar
  70. 70.
    Robbins SJ, Bussell RH. Structural phosphoproteins associated with purified measles virions and cytoplasmic nucleocapsids. Intervirology 1979; 12:96–102.PubMedCrossRefGoogle Scholar
  71. 71.
    Robbins SJ, Bussell RH, Rapp F. Isolation and partial characterization of two forms of cytoplasmic nucleocapsids from measles virus-infected cells. J Gen Virol 1980; 47:301–310.PubMedCrossRefGoogle Scholar
  72. 72.
    Stallcup KC, Wechsler SL, Fields BN. Purification of measles virus and characterization of subviral components. J Virol 1979; 30:166–176.PubMedGoogle Scholar
  73. 73.
    Vasconcelos D, Norrby E, Oglesbee M. The cellular stress response increases measles virus-induced cytopathic effect. J Gen Virol 1998; 79:1769–1773.PubMedGoogle Scholar
  74. 74.
    Vasconcelos DY, Cai XH, Oglesbee MJ. 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.PubMedGoogle Scholar
  75. 75.
    Oglesbee MJ, Kenney H, Kenney T et al. Enhanced production of morbillivirus gene-specific RNAs following induction of the cellular stress response in stable persistent infection. Virology 1993; 192:556–567.PubMedCrossRefGoogle Scholar
  76. 76.
    Oglesbee MJ, Liu Z, Kenney H et al. 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.PubMedCrossRefGoogle Scholar
  77. 77.
    Carsillo T, Zhang X, Vasconcelos D et al. 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.PubMedCrossRefGoogle Scholar
  78. 78.
    Oglesbee M. Nucleocapsid protein interactions with the major inducible 70 kDa heat shock protein. In: Longhi S, ed. Measles virus nucleoprotein. Hauppage, NY: Nova Publishers Inc., 2007:53–98.Google Scholar
  79. 79.
    Tsai CD, Ma B, Kumar S et al. Protein folding: binding of conformationally fluctuating building blocks via population selection. Crit Rev Biochem Mol Biol 2001; 36:399–433.PubMedCrossRefGoogle Scholar
  80. 80.
    Tsai CJ, Ma B, Sham YY et al. Structured disorder and conformational selection. Proteins: Structure, Function and Bioinformatics 2001; 44:418–427.CrossRefGoogle Scholar
  81. 81.
    Shoemaker BA, Portman JJ, Wolynes PG. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc Natl Acad Sci USA 2000; 97:8868–8873.PubMedCrossRefGoogle Scholar
  82. 82.
    Tarbouriech N, Curran J, Ruigrok RW et al. Tetrameric coiled coil domain of Sendai virus phosphoprotein. Nat Struct Biol 2000; 7:777–781.PubMedCrossRefGoogle Scholar
  83. 83.
    DeLano WL. The PyMOL molecular graphics system Proteins: Structure, Function and Bioinformatics 2002; 30:442–454.Google Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2012

Authors and Affiliations

  • Sonia Longhi
    • 1
  1. 1.Architecture et Fonction des Macromolécules BiologiquesUniversités d’Aix-Marseille I et IIMarseilleFrance

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