Skip to main content
SpringerLink
Log in

Order and Disorder in the Replicative Complex of Paramyxoviruses

  • Chapter
  • First Online:
Intrinsically Disordered Proteins Studied by NMR Spectroscopy

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 870))

Abstract

In this review we summarize available data showing the abundance of structural disorder within the nucleoprotein (N) and phosphoprotein (P) from three paramyxoviruses, namely the measles (MeV), Nipah (NiV) and Hendra (HeV) viruses. We provide a detailed description of the molecular mechanisms that govern the disorder-to-order transition that the intrinsically disordered C-terminal domain (NTAIL) of their N proteins undergoes upon binding to the C-terminal X domain (XD) of the homologous P proteins. We also show that a significant flexibility persists within NTAIL–XD complexes, which therefore provide illustrative examples of “fuzziness”. The functional implications of structural disorder for viral transcription and replication are discussed in light of the ability of disordered regions to establish a complex molecular partnership and to confer a considerable reach to the elements of the replicative machinery.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Albertini AAV, Schoehn G, Ruigrok RW (2005) Structures impliquées dans la réplication et la transcription des virus à ARN non segmentés de sens négatif. Virologie 9:83–92

    Google Scholar 

  • Audsley MD, Moseley GW (2013) Paramyxovirus evasion of innate immunity: diverse strategies for common targets. World J Virol 2:57–70

    Article  PubMed Central  PubMed  Google Scholar 

  • Balazs A, Csizmok V, Buday L et al (2009) High levels of structural disorder in scaffold proteins as exemplified by a novel neuronal protein, CASK-interactive protein1. FEBS J 276:3744–3756

    Article  CAS  PubMed  Google Scholar 

  • Bankamp B, Horikami SM, Thompson PD et al (1996) Domains of the measles virus N protein required for binding to P protein and self-assembly. Virology 216:272–277

    Article  CAS  PubMed  Google Scholar 

  • Baronti L, Erales J, Habchi J et al (2015) 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 6:268–276

    Article  CAS  Google Scholar 

  • Belle V, Rouger S, Costanzo S et al (2008) Mapping α-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 73:973–988

    Article  CAS  Google Scholar 

  • Bernadό P, Blanchard L, Timmins P et al (2005) A structural model for unfolded proteins from residual dipolar couplings and small-angle x-ray scattering. Proc Natl Acad Sci U S A 102:17002–17007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bhella D (2007) Measles virus nucleocapsid structure, conformational flexibility and the rule of six. In: Longhi S (ed) Measles virus nucleoprotein. Nova Publishers Inc., Hauppage

    Google Scholar 

  • Bhella D, Ralph A, Murphy LB et al (2002) Significant differences in nucleocapsid morphology within the Paramyxoviridae. J Gen Virol 83:1831–1839

    Article  CAS  PubMed  Google Scholar 

  • Bhella D, Ralph A, Yeo RP (2004) Conformational flexibility in recombinant measles virus nucleocapsids visualised by cryo-negative stain electron microscopy and real-space helical reconstruction. J Mol Biol 340:319–331

    Article  CAS  PubMed  Google Scholar 

  • Bischak CG, Longhi S, Snead DM et al (2010) Probing structural transitions in the intrinsically disordered C-terminal domain of the measles virus nucleoprotein by vibrational spectroscopy of cyanylated cysteines. Biophys J 99:1676–1683

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blanchard L, Tarbouriech N, Blackledge M et al (2004) Structure and dynamics of the nucleocapsid-binding domain of the Sendai virus phosphoprotein in solution. Virology 319:201–211

    Article  CAS  PubMed  Google Scholar 

  • Blocquel D, Bourhis JM, Eléouët JF et al (2012a) Transcription et réplication des Mononégavirales: une machine moléculaire originale. Virologie 16:225–257

    Google Scholar 

  • Blocquel D, Habchi J, Costanzo S et al (2012b) Interaction between the C-terminal domains of measles virus nucleoprotein and phosphoprotein: A tight complex implying one binding site. Protein Sci 21:1577–1585

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blocquel D, Habchi J, Gruet A et al (2012c) Compaction and binding properties of the intrinsically disordered C-terminal domain of Henipavirus nucleoprotein as unveiled by deletion studies. Mol Biosyst 8:392–410

    Article  CAS  PubMed  Google Scholar 

  • Blocquel D, Beltrandi M, Erales J et al (2013) Biochemical and structural studies of the oligomerization domain of the Nipah virus phosphoprotein: Evidence for an elongated coiled-coil homotrimer. Virology 446:162–172

    Article  CAS  PubMed  Google Scholar 

  • Blocquel D, Habchi J, Durand E et al (2014) Coiled-coil deformations in crystal structures: the measles virus phosphoprotein multimerization domain as an illustrative example. Acta Cryst D 70:1589–1603

    Article  CAS  Google Scholar 

  • Bourhis J, Johansson K, Receveur-Bréchot V et al (2004) The C-terminal domain of measles virus nucleoprotein belongs to the class of intrinsically disordered proteins that fold upon binding to their physiological partner. Virus Res 99:157–167

    Article  CAS  PubMed  Google Scholar 

  • Bourhis JM, Receveur-Bréchot V, Oglesbee M et al (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 Sci 14:1975–1992

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bourhis JM, Canard B, Longhi S (2007) Predicting protein disorder and induced folding: from theoretical principles to practical applications. Curr Protein Pept Sci 8:135–149

    Article  CAS  PubMed  Google Scholar 

  • Bruhn-Johannsen JF, Barnett K, Bibby J et al (2014) Crystal structure of the Nipah virus phosphoprotein tetramerization domain. J Virol 88:758–762

    Article  CAS  Google Scholar 

  • Buchholz CJ, Spehner D, Drillien R et al (1993) The conserved N-terminal region of Sendai virus nucleocapsid protein NP is required for nucleocapsid assembly. J Virol 67:5803–5812

    PubMed Central  CAS  PubMed  Google Scholar 

  • Buchholz CJ, Retzler C, Homann HE et al (1994) The carboxy-terminal domain of Sendai virus nucleocapsid protein is involved in complex formation between phosphoprotein and nucleocapsid- like particles. Virology 204:770–776

    Article  CAS  PubMed  Google Scholar 

  • Campen A, Williams RM, Brown CJ et al (2008) TOP-IDP-scale: a new amino acid scale measuring propensity for intrinsic disorder. Protein Pept Lett 15:956–963

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carsillo T, Traylor Z, Choi C et al (2006a) hsp72, a host determinant of measles virus neurovirulence. J Virol 80:11031–11039

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carsillo T, Zhang X, Vasconcelos D et al (2006b) A single codon in the nucleocapsid protein C terminus contributes to in vitro and in vivo fitness of Edmonston measles virus. J Virol 80:2904–2912

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chattopadhyay S, Banerjee AK (2009) Phosphoprotein, P of human parainfluenza virus type 3 prevents self-association of RNA-dependent RNA polymerase, L. Virology 383:226–236

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen M, Cortay JC, Gerlier D (2003) Measles virus protein interactions in yeast: new findings and caveats. Virus Res 98:123–129

    Article  CAS  PubMed  Google Scholar 

  • Chen JW, Romero P, Uversky VN et al (2006) Conservation of intrinsic disorder in protein domains and families: I. A database of conserved predicted disordered regions. J Proteome Res 5:879–887

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Colombo M, Bourhis JM, Chamontin C et al (2009) The interaction between the measles virus nucleoprotein and the Interferon Regulator Factor 3 relies on a specific cellular environment. Virol J 6:59

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Communie G, Crepin T, Maurin D et al (2013a) Structure of the tetramerization domain of measles virus phosphoprotein. J Virol 87:7166–7169

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Communie G, Habchi J, Yabukarski F et al (2013b) Atomic resolution description of the interaction between the nucleoprotein and phosphoprotein of Hendra virus. PLoS Pathog 9:e1003631

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cortese MS, Uversky VN, Dunker AK (2008) Intrinsic disorder in scaffold proteins: getting more from less. Prog Biophys Mol Biol 98:85–106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Couturier M, Buccellato M, Costanzo S et al (2010) High Affinity Binding between Hsp70 and the C-Terminal Domain of the Measles Virus Nucleoprotein Requires an Hsp40 Co-Chaperone. J Mol Recognit 23:301–315

    CAS  PubMed  Google Scholar 

  • Cox R, Green TJ, Purushotham S et al (2013) Structural and functional characterization of the mumps virus phosphoprotein. J Virol 87:7558–7568

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Curran J (1998) A role for the Sendai virus P protein trimer in RNA synthesis. J Virol 72:4274–4280

    PubMed Central  CAS  PubMed  Google Scholar 

  • Curran J, Homann H, Buchholz C et al (1993) The hypervariable C-terminal tail of the Sendai paramyxovirus nucleocapsid protein is required for template function but not for RNA encapsidation. J Virol 67:4358–4364

    PubMed Central  CAS  PubMed  Google Scholar 

  • Curran J, Pelet T, Kolakofsky D (1994) An acidic activation-like domain of the Sendai virus P protein is required for RNA synthesis and encapsidation. Virology 202:875–884

    Article  CAS  PubMed  Google Scholar 

  • Curran J, Boeck R, Lin-Marq N et al (1995a) Paramyxovirus phosphoproteins form homotrimers as determined by an epitope dilution assay, via predicted coiled coils. Virology 214:139–149

    Article  CAS  PubMed  Google Scholar 

  • Curran J, Marq JB, Kolakofsky D (1995b) 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 69:849–855

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dahlman-Wright K, McEwan IJ (1996) Structural studies of mutant glucocorticoid receptor transactivation domains establish a link between transactivation activity in vivo and α-helix-forming potential in vitro. BioChemistry 35:1323–1327

    Article  CAS  PubMed  Google Scholar 

  • Davey NE, Trave G, Gibson TJ (2011) How viruses hijack cell regulation. Trends Biochem Sci 36:159–169

    Article  CAS  PubMed  Google Scholar 

  • Davey NE, Van Roey K, Weatheritt RJ et al (2012) Attributes of short linear motifs. Mol Biosyst 8:268–281

    Article  CAS  PubMed  Google Scholar 

  • De BP, Banerjee AK (1999) Involvement of actin microfilaments in the transcription/replication of human parainfluenza virus type 3: possible role of actin in other viruses. Microsc Res Tech 47:114–123

    Article  CAS  PubMed  Google Scholar 

  • DeLano WL (2002) The PyMOL molecular graphics system. Proteins: Struct Funct Bioinform 30:442–454

    Google Scholar 

  • Desfosses A, Goret G, Farias Estrozi L et al (2011) Nucleoprotein-RNA orientation in the measles virus nucleocapsid by three-dimensional electron microscopy. J Virol 85:1391–1395

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Diallo A, Barrett T, Barbron M et al (1994) Cloning of the nucleocapsid protein gene of peste-des-petits-ruminants virus: relationship to other morbilliviruses. J Gen Virol 75(1):233–237

    Article  CAS  PubMed  Google Scholar 

  • Ding B, Zhang G, Yang X et al (2014) Phosphoprotein of human parainfluenza virus type 3 blocks autophagosome-lysosome fusion to increase virus production. Cell Host Microbe 15:564–577

    Article  CAS  PubMed  Google Scholar 

  • Dunker AK, Lawson JD, Brown CJ et al (2001) Intrinsically disordered protein. J Mol Graph Model 19:26–59

    Article  CAS  PubMed  Google Scholar 

  • Dunker AK, Cortese MS, Romero P et al (2005) Flexible nets. FEBS J 272:5129–5148

    Article  CAS  PubMed  Google Scholar 

  • Dutta K, Alexandrov A, Huang H et al (2001) pH-induced folding of an apoptotic coiled coil. Protein Sci 10:2531–2540

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Espinoza-Fonseca LM (2009) Reconciling binding mechanisms of intrinsically disordered proteins. Biochem Biophys Res Commun 382:479–482

    Article  CAS  PubMed  Google Scholar 

  • Ferron F, Longhi S, Henrissat B et al (2002) Viral RNA-polymerases—a predicted 2’-O-ribose methyltransferase domain shared by all Mononegavirales. Trends Biochem Sci 27:222–224

    Article  CAS  PubMed  Google Scholar 

  • Ferron F, Longhi S, Canard B et al (2006) A practical overview of protein disorder prediction methods. Proteins 65:1–14

    Article  CAS  PubMed  Google Scholar 

  • Fontana JM, Bankamp B, Rota PA (2008) Inhibition of interferon induction and signaling by paramyxoviruses. Immunol Rev 225:46–67

    Article  CAS  PubMed  Google Scholar 

  • Garner E, Romero P, Dunker AK et al (1999) Predicting binding regions within disordered proteins. Genome Inform Ser Workshop Genome Inform 10:41–50

    CAS  PubMed  Google Scholar 

  • Gely S, Lowry DF, Bernard C et al (2010) 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 23:435–447

    Article  CAS  PubMed  Google Scholar 

  • Gopinath M, Shaila MS (2008) Recombinant L and P protein complex of Rinderpest virus catalyses mRNA synthesis in vitro. Virus Res 135:150–154

    Article  CAS  PubMed  Google Scholar 

  • Gruet A, Longhi S, Bignon C (2012) One-step generation of error-prone PCR libraries using Gateway(R) technology. Microb Cell Fact 11:14

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gruet A, Dosnon M, Vassena A et al (2013) Dissecting partner recognition by an intrinsically disordered protein using descriptive random mutagenesis. J Mol Biol 425:3495–3509

    Article  CAS  PubMed  Google Scholar 

  • Habchi J, Longhi S (2012) Structural disorder within paramyxovirus nucleoproteins and phosphoproteins. Mol Biosyst 8:69–81

    Article  CAS  PubMed  Google Scholar 

  • Habchi J, Mamelli L, Darbon H et al (2010) Structural disorder within Henipavirus nucleoprotein and phosphoprotein: from predictions to experimental assessment. PLoS ONE 5:e11684

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Habchi J, Blangy S, Mamelli L et al (2011) Characterization of the interactions between the nucleoprotein and the phosphoprotein of Henipaviruses. J Biol Chem 286:13583–13602

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Habchi J, Mamelli L, Longhi S (2012) Structural disorder within the nucleoprotein and phosphoprotein from measles, Nipah and Hendra viruses. In: Uversky VN, Longhi S (eds) Flexible viruses: structural disorder in viral proteins. Wiley, Hoboken, pp 47–94

    Google Scholar 

  • Habchi J, Tompa P, Longhi S et al (2014) Introducing protein intrinsic disorder. Chem Rev 114:6561–6588

    Article  CAS  PubMed  Google Scholar 

  • Haynes C, Oldfield CJ, Ji F et al (2006) Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput Biol 2:e100

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Heggeness MH, Scheid A, Choppin PW (1980) 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 U S A 77:2631–2635

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Heggeness MH, Scheid A, Choppin PW (1981) The relationship of conformational changes in the Sendai virus nucleocapsid to proteolytic cleavage of the NP polypeptide. Virology 114:555–562

    Article  CAS  PubMed  Google Scholar 

  • Houben K, Blanchard L, Blackledge M et al (2007a) Intrinsic dynamics of the partly unstructured PX domain from the Sendai virus RNA polymerase cofactor P. Biophys J 93:2830–2844

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Houben K, Marion D, Tarbouriech N et al (2007b) Interaction of the C-terminal domains of sendai virus N and P proteins: comparison of polymerase-nucleocapsid interactions within the paramyxovirus family. J Virol 81:6807–6816

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hua QX, Jia WH, Bullock BP et al (1998) Transcriptional activator-coactivator recognition: nascent folding of a kinase-inducible transactivation domain predicts its structure on coactivator binding. BioChemistry 37:5858–5866

    Article  CAS  PubMed  Google Scholar 

  • Huber M, Cattaneo R, Spielhofer P et al (1991) Measles virus phosphoprotein retains the nucleocapsid protein in the cytoplasm. Virology 185:299–308

    Article  CAS  PubMed  Google Scholar 

  • Iwasaki M, Takeda M, Shirogane Y et al (2009) The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J Virol 83:10374–10383

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jensen MR, Houben K, Lescop E et al (2008) Quantitative conformational analysis of partially folded proteins from residual dipolar couplings: application to the molecular recognition element of Sendai virus nucleoprotein. J Am Chem Soc 130:8055–8061

    Article  CAS  PubMed  Google Scholar 

  • Jensen MR, Bernadό P, Houben K et al (2010) Structural disorder within sendai virus nucleoprotein and phosphoprotein: insight into the structural basis of molecular recognition. Protein Pept Lett 17:952–960

    Article  CAS  PubMed  Google Scholar 

  • Johansson K, Bourhis JM, Campanacci V et al (2003) Crystal structure of the measles virus phosphoprotein domain responsible for the induced folding of the C-terminal domain of the nucleoprotein. J Biol Chem 278:44567–44573

    Article  CAS  PubMed  Google Scholar 

  • Jordan IK, Sutter BA, McClure MA (2000) Molecular evolution of the Paramyxoviridae and Rhabdoviridae multiple-protein-encoding P gene. Mol Biol Evol 17:75–86

    Article  CAS  PubMed  Google Scholar 

  • Karlin D, Belshaw R (2012) Detecting remote sequence homology in disordered proteins: discovery of conserved motifs in the N-termini of Mononegavirales phosphoproteins. PLoS ONE 7:e31719

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karlin D, Longhi S, Canard B (2002a) Substitution of two residues in the measles virus nucleoprotein results in an impaired self-association. Virology 302:420–432

    Article  CAS  PubMed  Google Scholar 

  • Karlin D, Longhi S, Receveur V et al (2002b) The N-terminal domain of the phosphoprotein of morbilliviruses belongs to the natively unfolded class of proteins. Virology 296:251–262

    Article  CAS  PubMed  Google Scholar 

  • Karlin D, Ferron F, Canard B et al (2003) Structural disorder and modular organization in Paramyxovirinae N and P. J Gen Virol 84:3239–3252

    Article  CAS  PubMed  Google Scholar 

  • Kavalenka A, Urbancic I, Belle V et al (2010) Conformational analysis of the partially disordered measles virus NTAIL-XD complex by SDSL EPR spectroscopy. Biophys J 98:1055–1064

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kerdiles YM, Cherif B, Marie JC et al (2006) Immunomodulatory properties of morbillivirus nucleoproteins. Viral Immunol 19:324–334

    Article  CAS  PubMed  Google Scholar 

  • Kingston RL, Hamel DJ, Gay LS et al (2004a) Structural basis for the attachment of a paramyxoviral polymerase to its template. Proc Natl Acad Sci U S A 101:8301–8306

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kingston RL, Walter AB, Gay LS (2004b) Characterization of nucleocapsid binding by the measles and the mumps virus phosphoprotein. J Virol 78:8630–8640

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kingston RL, Gay LS, Baase WS et al (2008) Structure of the nucleocapsid-binding domain from the mumps virus polymerase; an example of protein folding induced by crystallization. J Mol Biol 379:719–731

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kiss R, Bozoky Z, Kovacs D et al (2008) Calcium-induced tripartite binding of intrinsically disordered calpastatin to its cognate enzyme, calpain. FEBS Lett 582:2149–2154

    Article  CAS  PubMed  Google Scholar 

  • Kolakofsky D, Pelet T, Garcin D et al (1998) Paramyxovirus RNA synthesis and the requirement for hexamer genome length: the rule of six revisited. J Virol 72:891–899

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kolakofsky D, Le Mercier P, Iseni F et al (2004) Viral DNA polymerase scanning and the gymnastics of Sendai virus RNA synthesis. Virology 318:463–473

    Article  CAS  PubMed  Google Scholar 

  • Kovacs E, Tompa P, Liliom K et al (2010) Dual coding in alternative reading frames correlates with intrinsic protein disorder. Proc Natl Acad Sci U S A 107:5429–5434

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Krumm SA, Takeda M, Plemper RK (2013) The measles virus nucleocapsid protein tail domain is dispensable for viral polymerase recruitment and activity. J Biol Chem 288:29943–29953

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Laine D, Trescol-Biémont M, Longhi S et al (2003) 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 77:11332–11346

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Laine D, Bourhis J, Longhi S et al (2005) Measles virus nucleoprotein induces cell proliferation arrest and apoptosis through NTAIL/NR and NCORE/FcgRIIB1 interactions, respectively. J Gen Virol 86:1771–1784

    Article  CAS  PubMed  Google Scholar 

  • Laine D, Vidalain P, Gahnnam A et al (2007) Interaction of measles virus nucleoprotein with cell surface receptors: impact on cell biology and immune response. In: Longhi S (ed) Measles virus nucleoprotein. Nova Publishers Inc., Hauppage, pp 113–152

    Google Scholar 

  • Lamb RA, Kolakofsky D (2001) Paramyxoviridae: the viruses and their replication. In: Fields BN, Knipe DM, Howley PM (eds) Fields virology, 4th edn. Lippincott-Raven, Philadelphia, pp 1305–1340

    Google Scholar 

  • Lamb RA, Parks GD (2007) Paramyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM (eds) Fields virology, 5th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1450–1497

    Google Scholar 

  • Leyrat C, Gerard FC, de Almeida Ribeiro E Jr et al (2010) Structural disorder in proteins of the rhabdoviridae replication complex. Protein Pept Lett 17:979–987

    Article  CAS  PubMed  Google Scholar 

  • Leyrat C, Jensen MR, Ribeiro EA Jr et al (2011a) The N(0)-binding region of the vesicular stomatitis virus phosphoprotein is globally disordered but contains transient αhelices. Protein Sci 20:542–556

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leyrat C, Yabukarski F, Tarbouriech N et al (2011b) Structure of the vesicular stomatitis virus N(0)-P complex. PLoS Pathog 7:e1002248

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lieutaud P, Canard B, Longhi S (2008) MeDor: a metaserver for predicting protein disorder. BMC Genomics 9:S25

    Article  PubMed Central  PubMed  Google Scholar 

  • Lieutaud P, Ferron F, Habchi J et al (2013) Predicting protein disorder and induced folding: a practical approach. In: Dunn B (ed) Advances in protein and peptide sciences. Bentham Science Publishers, Sharjah, pp 441–492 (52)

    Chapter  Google Scholar 

  • Liston P, DiFlumeri C, Briedis DJ (1995) Protein interactions entered into by the measles virus P, V, and C proteins. Virus Res 38:241–259

    Article  CAS  PubMed  Google Scholar 

  • Liston P, Batal R, DiFlumeri C et al (1997) Protein interaction domains of the measles virus nucleocapsid protein (NP). Arch Virol 142:305–321

    Article  CAS  PubMed  Google Scholar 

  • Llorente MT, Barreno-Garcia B, Calero M et al (2006) Structural analysis of the human respiratory syncitial virus phosphoprotein: characterization of an a-helical domain involved in oligomerization. J Gen Virol 87:159–169

    Article  CAS  PubMed  Google Scholar 

  • Llorente MT, Taylor IA, Lopez-Vinas E et al (2008) Structural properties of the human respiratory syncytial virus P protein: evidence for an elongated homotetrameric molecule that is the smallest orthologue within the family of paramyxovirus polymerase cofactors. Proteins 72:946–958

    Article  CAS  PubMed  Google Scholar 

  • Longhi S (ed) (2007) Measles virus nucleoprotein. Nova Publishers Inc., Hauppage

    Google Scholar 

  • Longhi S (2009) Nucleocapsid structure and function. Curr Top Microbiol Immunol 329:103–128

    CAS  PubMed  Google Scholar 

  • Longhi S (2011) Structural disorder within the measles virus nucleoprotein and phosphoprotein: functional implications for transcription and replication. In: Luo M (ed) Negative strand RNA virus. World Scientific Publishing, Singapore, pp 95–125

    Chapter  Google Scholar 

  • Longhi S, Canard B (1999) Mécanismes de transcription et de réplication des Paramyxoviridae. Virologie 3:227–240

    Google Scholar 

  • Longhi S, Oglesbee M (2010) Structural disorder within the measles virus nucleoprotein and phosphoprotein. Protein Pept Lett 17:961–978

    Article  CAS  PubMed  Google Scholar 

  • Longhi S, Receveur-Brechot V, Karlin D et al (2003) 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 278:18638–18648

    Article  CAS  PubMed  Google Scholar 

  • Longhi S, Lieutaud P, Canard B (2010) Conformational disorder. Methods Mol Biol 609:307–325

    Article  CAS  PubMed  Google Scholar 

  • Lupas AN, Gruber M (2005) The structure of αhelical coiled coils. Adv Protein Chem 70:37–78

    Article  CAS  PubMed  Google Scholar 

  • Magliery TJ, Wilson CG, Pan W et al (2005) Detecting protein-protein interactions with a green fluorescent protein fragment reassembly trap: scope and mechanism. J Am Chem Soc 127:146–157

    Article  CAS  PubMed  Google Scholar 

  • Martinho M, Habchi J, El Habre Z et al (2013) 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 31:453–471

    Article  CAS  PubMed  Google Scholar 

  • Meszaros B, Tompa P, Simon I et al (2007) Molecular principles of the interactions of disordered proteins. J Mol Biol 372:549–561

    Article  CAS  PubMed  Google Scholar 

  • Mittag T, Orlicky S, Choy WY et al (2008) Dynamic equilibrium engagement of a polyvalent ligand with a single-site receptor. Proc Natl Acad Sci U S A 105:17772–17777

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mohan A, Oldfield CJ, Radivojac P et al (2006) Analysis of molecular recognition features (MoRFs). J Mol Biol 362:1043–1059

    Article  CAS  PubMed  Google Scholar 

  • Morin B, Bourhis JM, Belle V et al (2006) Assessing induced folding of an intrinsically disordered protein by site-directed spin-labeling EPR spectroscopy. J Phys Chem B 110:20596–20608

    Article  CAS  PubMed  Google Scholar 

  • Moyer SA, Baker SC, Horikami SM (1990) Host cell proteins required for measles virus reproduction. J Gen Virol 71:775–783

    Article  CAS  PubMed  Google Scholar 

  • Myers TM, Pieters A, Moyer SA (1997) A highly conserved region of the Sendai virus nucleocapsid protein contributes to the NP-NP binding domain. Virology 229:322–335

    Article  CAS  PubMed  Google Scholar 

  • Myers TM, Smallwood S, Moyer SA (1999) Identification of nucleocapsid protein residues required for Sendai virus nucleocapsid formation and genome replication. J Gen Virol 80:1383–1391

    Article  CAS  PubMed  Google Scholar 

  • Narechania A, Terai M, Burk RD (2005) Overlapping reading frames in closely related human papillomaviruses result in modular rates of selection within E2. J Gen Virol 86:1307–1313

    Article  CAS  PubMed  Google Scholar 

  • Ogino T, Kobayashi M, Iwama M et al (2005) Sendai virus RNA-dependent RNA polymerase L protein catalyzes cap methylation of virus-specific mRNA. J Biol Chem 280:4429–4435

    Article  CAS  PubMed  Google Scholar 

  • Oglesbee M (2007) Nucleocapsid protein interactions with the major inducible heat shock protein. In: Longhi S (ed) Measles virus nucleoprotein. Nova Publishers Inc., Hauppage, pp 53–98

    Google Scholar 

  • Oglesbee M, Tatalick L, Rice J et al (1989) Isolation and characterization of canine distemper virus nucleocapsid variants. J Gen Virol 70(9):2409–2419

    Article  CAS  PubMed  Google Scholar 

  • Oglesbee M, Ringler S, Krakowka S (1990) Interaction of canine distemper virus nucleocapsid variants with 70K heat-shock proteins. J Gen Virol 71:1585–1590

    Article  CAS  PubMed  Google Scholar 

  • Oglesbee MJ, Kenney H, Kenney T et al (1993) Enhanced production of morbillivirus gene-specific RNAs following induction of the cellular stress response in stable persistent infection. Virology 192:556–567

    Article  CAS  PubMed  Google Scholar 

  • Oglesbee MJ, Liu Z, Kenney H et al (1996) The highly inducible member of the 70kDa family of heat shock proteins increases canine distemper virus polymerase activity. J Gen Virol 77:2125–2135

    Article  CAS  PubMed  Google Scholar 

  • Oldfield CJ, Cheng Y, Cortese MS et al (2005) Coupled folding and binding with α-helix-forming molecular recognition elements. Biochemistry 44:12454–12470

    Article  CAS  PubMed  Google Scholar 

  • Oshaben KM, Salari R, McCaslin DR et al (2012) The native GCN4 leucine-zipper domain does not uniquely specify a dimeric oligomerization state. BioChemistry 51:9581–9591

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Park MS, Shaw ML, Munoz-Jordan J et al (2003) Newcastle disease virus (NDV)-based assay demonstrates interferon-antagonist activity for the NDV V protein and the Nipah virus V, W, and C proteins. J Virol 77:1501–1511

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rahaman A, Srinivasan N, Shamala N et al (2004) Phosphoprotein of the rinderpest virus forms a tetramer through a coiled coil region important for biological function. A structural insight. J Biol Chem 279:23606–23614

    Article  CAS  PubMed  Google Scholar 

  • Rancurel C, Khosravi M, Dunker KA et al (2009) Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J Virol 83:10719–10736

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ringkjøbing Jensen M, Communie G, Ribeiro ED Jr et al (2011) Intrinsic disorder in measles virus nucleocapsids. Proc Natl Acad Sci U S A 108:9839–9844

    Article  Google Scholar 

  • Romero PR, Zaidi S, Fang YY et al (2006) Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proc Natl Acad Sci U S A 103:8390–8395

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roux L (2005) Dans le génome des Paramyxovirinae, les promoteurs et leurs activités sont façonnés par la “règle de six”. Virologie 9:19–34

    Google Scholar 

  • Rudolph MG, Kraus I, Dickmanns A et al (2003) Crystal structure of the borna disease virus nucleoprotein. Structure (Camb) 11:1219–1226

    Article  CAS  Google Scholar 

  • Ryan KW, Portner A (1990) Separate domains of Sendai virus P protein are required for binding to viral nucleocapsids. Virology 174:515–521

    Article  CAS  PubMed  Google Scholar 

  • Salvamani S, Goh Z, Ho K et al (2013) Oligomerization state of the multimerization domain of Nipah virus phosphoprotein. Process Biochem 48:1476–1480

    Article  CAS  Google Scholar 

  • Sato H, Masuda M, Miura R et al (2006) Morbillivirus nucleoprotein possesses a novel nuclear localization signal and a CRM1-independent nuclear export signal. Virology 352:121–130

    Article  CAS  PubMed  Google Scholar 

  • Schoehn G, Mavrakis M, Albertini A et al (2004) The 12A structure of trypsin-treated measles virus N-RNA. J Mol Biol 339:301–312

    Article  CAS  PubMed  Google Scholar 

  • Shoemaker BA, Portman JJ, Wolynes PG (2000) Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc Natl Acad Sci U S A 97:8868–8873

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shu Y, Habchi J, Costanzo S et al (2012) Plasticity in structural and functional interactions between the phosphoprotein and nucleoprotein of measles virus. J Biol Chem 287:11951–11967

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Spehner D, Kirn A, Drillien R (1991) Assembly of nucleocapsidlike structures in animal cells infected with a vaccinia virus recombinant encoding the measles virus nucleoprotein. J Virol 65:6296–6300

    PubMed Central  CAS  PubMed  Google Scholar 

  • Spehner D, Drillien R, Howley PM (1997) The assembly of the measles virus nucleoprotein into nucleocapsid-like particles is modulated by the phosphoprotein. Virology 232:260–268

    Article  CAS  PubMed  Google Scholar 

  • Sue SC, Cervantes C, Komives EA et al (2008) Transfer of flexibility between ankyrin repeats in IkappaB* upon formation of the NF-kappaB complex. J Mol Biol 380:917–931

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sweetman DA, Miskin J, Baron MD (2001) Rinderpest virus C and V proteins interact with the major (L) component of the viral polymerase. Virology 281:193–204

    Article  CAS  PubMed  Google Scholar 

  • Tan WS, Ong ST, Eshaghi M et al (2004) Solubility, immunogenicity and physical properties of the nucleocapsid protein of Nipah virus produced in Escherichia coli. J Med Virol 73:105–112

    Article  CAS  PubMed  Google Scholar 

  • Tapparel C, Maurice D, Roux L (1998) 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 72:3117–3128

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tarbouriech N, Curran J, Ruigrok RW et al (2000) Tetrameric coiled coil domain of Sendai virus phosphoprotein. Nat Struct Biol 7:777–781

    Article  CAS  PubMed  Google Scholar 

  • Tawar RG, Duquerroy S, Vonrhein C et al (2009) 3D structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326:1279–1283

    Article  CAS  PubMed  Google Scholar 

  • tenOever BR, Servant MJ, Grandvaux N et al (2002) Recognition of the Measles Virus Nucleocapsid as a Mechanism of IRF-3 Activation. J Virol 76:3659–3669

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tokuriki N, Oldfield CJ, Uversky VN et al (2009) Do viral proteins possess unique biophysical features? Trends Biochem Sci 34:53–59

    Article  CAS  PubMed  Google Scholar 

  • Tompa P, Fuxreiter M (2008) Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem Sci 33:2–8

    Article  CAS  PubMed  Google Scholar 

  • Tran TL, Castagne N, Bhella D et al (2007) The nine C-terminal amino acids of the respiratory syncytial virus protein P are necessary and sufficient for binding to ribonucleoprotein complexes in which six ribonucleotides are contacted per N protein protomer. J Gen Virol 88:196–206

    Article  CAS  PubMed  Google Scholar 

  • Tsai CD, Ma B, Kumar S et al (2001a) Protein folding: binding of conformationally fluctuating building blocks via population selection. Crit Rev Biochem Mol Biol 36:399–433

    Article  CAS  PubMed  Google Scholar 

  • Tsai CD, Ma B, Sham YY et al (2001b) Structured disorder and conformational selection. Proteins: structure. Funct Bioinform 44:418–427

    Google Scholar 

  • Ulane CM, Horvath CM (2002) Paramyxoviruses SV5 and HPIV2 assemble STAT protein ubiquitin ligase complexes from cellular components. Virology 304:160–166

    Article  CAS  PubMed  Google Scholar 

  • Uversky VN (2002) Natively unfolded proteins: a point where biology waits for physics. Protein Sci 11:739–756

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Uversky VN, Longhi S (eds) (2012) Flexible viruses: structural disorder in viral proteins. Wiley, Hoboken

    Google Scholar 

  • Uversky VN, Oldfield CJ, Dunker AK (2005) Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling. J Mol Recognit 18:343–384

    Article  CAS  PubMed  Google Scholar 

  • Vacic V, Oldfield CJ, Mohan A et al (2007) Characterization of molecular recognition features, MoRFs, and their binding partners. J Proteome Res 6:2351–2366

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vasconcelos D, Norrby E, Oglesbee M (1998a) The cellular stress response increases measles virus-induced cytopathic effect. J Gen Virol 79:1769–1773

    Article  CAS  PubMed  Google Scholar 

  • Vasconcelos DY, Cai XH, Oglesbee MJ (1998b) Constitutive overexpression of the major inducible 70kDa heat shock protein mediates large plaque formation by measles virus. J Gen Virol 79:2239–2247

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Chu X, Longhi S et al (2013) Multiscaled exploration of coupled folding and binding of an intrinsically disordered molecular recognition element in measles virus nucleoprotein. Proc Natl Acad Sci U S A 110:E3743–E3752

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Warnes A, Fooks AR, Dowsett AB et al (1995) Expression of the measles virus nucleoprotein gene in Escherichia coli and assembly of nucleocapsid-like structures. Gene 160:173–178

    Article  CAS  PubMed  Google Scholar 

  • Watanabe N, Kawano M, Tsurudome M et al (1996) Identification of the sequences responsible for nuclear targeting of the V protein of human parainfluenza virus type 2. J Gen Virol 77:327–338

    Article  CAS  PubMed  Google Scholar 

  • Watanabe A, Yoneda M, Ikeda F et al (2011) Peroxiredoxin 1 is required for efficient transcription and replication of measles virus. J Virol 85:2247–2253

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilson CG, Magliery TJ, Regan L (2004) Detecting protein-protein interactions with GFP-fragment reassembly. Nat Methods 1:255–262

    Article  CAS  PubMed  Google Scholar 

  • Xue B, Williams RW, Oldfield CJ et al (2010) Viral disorder or disordered viruses: do viral proteins possess unique features? Protein Pept Lett 17:932–951

    Article  CAS  PubMed  Google Scholar 

  • Xue B, Dunker AK, Uversky VN (2012) Orderly order in protein intrinsic disorder distribution: disorder in 3500 proteomes from viruses and the three domains of life. J Biomol Struct Dyn 30:137–149

    Article  CAS  PubMed  Google Scholar 

  • Xue B, Blocquel D, Habchi J et al (2014) Structural Disorder in Viral Proteins. Chem Rev 114:6880–6911

    Article  CAS  PubMed  Google Scholar 

  • Yegambaram K, Kingston RL (2010) The feet of the measles virus polymerase bind the viral nucleocapsid protein at a single site. Protein Sci 19:893–899

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yegambaram K, Bulloch EM, Kingston RL (2013) Protein domain definition should allow for conditional disorder. Protein Sci 22:1502–1518

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang X, Glendening C, Linke H et al (2002) Identification and characterization of a regulatory domain on the carboxyl terminus of the measles virus nucleocapsid protein. J Virol 76:8737–8746

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang X, Bourhis JM, Longhi S et al (2005) Hsp72 recognizes a P binding motif in the measles virus N protein C-terminus. Virology 337:162–174

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We wish to thank all our co-workers who were involved in the studies herein summarized. This work was carried out with the financial support of the Agence Nationale de la Recherche, specific programs “Physico-Chimie du Vivant”, ANR-08-PCVI-0020-01, and “ASTRID”, ANR-11-ASTR-003-01. The work was also partly supported by the CNRS. D.B. was supported by a joint doctoral fellowship from the Direction Générale de l’Armement (DGA) and the CNRS. M.B. was partly supported by an Erasmus Master fellowship from the University of Milan and is presently supported by a Ph.D. fellowship from the French-Italian University. J.E. is supported by a post-doctoral fellowship from the Fondation pour la Recherche Médicale (FRM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Aix-Marseille Université, AFMB UMR 7257, 13288, Marseille, France

    Jenny Erales, David Blocquel, Johnny Habchi, Matilde Beltrandi, Antoine Gruet, Marion Dosnon, Christophe Bignon & Sonia Longhi

  2. CNRS, AFMB UMR 7257, 13288, Marseille, France

    Jenny Erales, David Blocquel, Johnny Habchi, Matilde Beltrandi, Antoine Gruet, Marion Dosnon, Christophe Bignon & Sonia Longhi

Authors
  1. Jenny Erales
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Blocquel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Johnny Habchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matilde Beltrandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Antoine Gruet
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marion Dosnon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Christophe Bignon
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sonia Longhi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sonia Longhi .

Editor information

Editors and Affiliations

  1. CERM and Department of Chemistry, "Ugo Schiff" University of Florence, Florence, Italy

    Isabella C. Felli

  2. CERM and Department of Chemistry, "Ugo Schiff" University of Florence, Florence, Italy

    Roberta Pierattelli

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Erales, J. et al. (2015). Order and Disorder in the Replicative Complex of Paramyxoviruses. In: Felli, I., Pierattelli, R. (eds) Intrinsically Disordered Proteins Studied by NMR Spectroscopy. Advances in Experimental Medicine and Biology, vol 870. Springer, Cham. https://doi.org/10.1007/978-3-319-20164-1_12

Download citation

Publish with us

Policies and ethics

Search

Navigation