The intrinsically disordered C-terminal domain of the measles virus nucleoprotein interacts with the C-terminal domain of the phosphoprotein via two distinct sites and remains predominantly unfolded

Protein Science

Volumn 14, Issue 8, 2005, Pages 1975-1992

  Bourhis, Jean Marie ^a   Receveur Bréchot, Véronique ^a   Oglesbee, Michael ^b   Zhang, Xinsheng ^b   Buccellato, Matthew ^b   Darbon, Hervé ^a   Canard, Bruno ^a   Finet, Stéphanie ^c   Longhi, Sonia ^a  

^a Centre National de la Recherche Scientifique   (France)

^b OHIO STATE UNIVERSITY   (United States)

^c EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

Author keywords

CD; Induced folding; Intrinsic disorder; Measles virus; NMR; Nucleoprotein; Phosphoprotein; SAXS

Indexed keywords

VIRUS NUCLEOPROTEIN; VIRUS PHOSPHOPROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BAY REGION BINDING SITE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; COMPLEX FORMATION; CONTROLLED STUDY; FLUORESCENCE SPECTROSCOPY; MEASLES VIRUS; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RADIATION SCATTERING; STRUCTURAL PROTEOMICS; SURFACE PLASMON RESONANCE;

BINDING SITES; CLONING, MOLECULAR; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEOPROTEINS; PHOSPHOPROTEINS; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SCATTERING, RADIATION; SEQUENCE DELETION; SPECTROMETRY, FLUORESCENCE; SURFACE PLASMON RESONANCE; VIRAL PROTEINS; X-RAYS;

HENDRA VIRUS; MEASLES VIRUS; MONONEGAVIRALES; RNA VIRUSES;

EID: 23644449725     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.051411805     Document Type: Article

References (79)

1. Bankamp, B., Horikami, S.M., Thompson, P.D., Huber, M., Billeter, M., and Moyer, S.A. 1996. Domains of the measles virus N protein required for binding to P protein and self-assembly. Virology 216: 272-277.
2. Bergmann, A., Fritz, G., and Glatter, O. 2000. Solving the generalized indirect Fourier transformation (GIFT) by Boltzmann simplex simulated annealing (BSSA). J. Appl. Crystallogr. 33: 1212-1216.
3. Bette, S., Breer, H., and Krieger, J. 2002. Probing a pheromone binding protein of the silkmoth Antheraea polyphemus by endogenous tryptophan fluorescence. Insect Biochem. Mol. Biol. 32: 241-246.
4. Bienkiewicz, E.A., Adkins, J.N., and Lumb, K.J. 2002. Functional consequences of preorganized helical structure in the intrinsically disordered cell-cycle inhibitor p27(Kip1). Biochemistry 41: 752-759.
5. Bourhis, J., Johansson, K., Receveur-Bréchot, V., Oldfield, C.J., Dunker, A.K., Canard, B., and Longhi, S. 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.
6. Brizzard, B.L., Chubet, R.G., and Vizard, D.L. 1994. Immunoaffinity purification of FLAG epitope-tagged bacterial alkaline phosphatase using a novel monoclonal antibody and peptide elution. Biotechniques 16: 730-735.
7. Buchholz, C.J., Spehner, D., Drillien, R., Neubert, W.J., and Homann, H.E. 1993. The conserved N-terminal region of Sendai virus nucleocapsid protein NP is required for nucleocapsid assembly. J. Virol. 67: 5803-5812.
8. Buckland, R., Giraudon, P., and Wild, F. 1989. Expression of measles virus nucleoprotein in Escherichia coli: Use of deletion mutants to locate the antigenic sites. J. Gen. Virol. 70: 435-441.
9. Coronel, E.C., Takimoto, T., Murti, K.G., Varich, N., and Portner, A. 2001. Nucleocapsid incorporation into parainfluenza virus is regulated by specific interaction with matrix protein. J. Virol. 75: 1117-1123.
10. Csizmok, V., Bokor, M., Banki, P., Klement, E., Medzihradszky, K.F., Friedrich, P., Tompa, K., and Tompa, P. 2005. Primary contact sites in intrinsically unstructured proteins: The case of calpastatin and microtubule-associated protein 2. Biochemistry 44: 3955-3964.
11. Curran, J. 1996. Reexamination of the Sendai virus P protein domains required for RNA synthesis: A possible supplemental role for the P protein. Virology 221: 130-140.
12. Curran, J. and Kolakofsky, D. 1999. Replication of paramyxoviruses. Adv. Virus Res. 54: 403-422.
13. Curran, J., Homann, H., Buchholz, C., Rochat, S., Neubert, W., and Kolakofsky, D. 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.
14. Curran, J., Pelet, T., and 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.
15. Curran, J., Boeck, R., Lin-Marq, N., Lupas, A., and Kolakofsky, D. 1995a. Paramyxovirus phosphoproteins form homotrimers as determined by an epitope dilution assay, via predicted coiled coils. Virology 214: 139-149.
16. Curran, J., Marq, J.B., and 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.
17. De, B.P. and Banerjee, A.K. 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.
18. De Guzman, R.N., Martinez-Yamout, M.A., Dyson, H.J., and Wright, P.E. 2004. Interaction of the TAZ1 domain of the CREB-binding protein with the activation domain of CITED2: Regulation by competition between intrinsically unstructured ligands for non-identical binding sites. J. Biol. Chem. 279: 3042-3049.
19. Diallo, A., Barrett, T., Barbron, M., Meyer, G., and Lefevre, P.C. 1994. Cloning of the nucleocapsid protein gene of peste-des-petits-ruminants virus: Relationship to other morbilliviruses. J. Gen. Virol. 75(Pt 1): 233-237.
20. Dunker, A.K. and Obradovic, Z. 2001. The protein trinity - Linking function and disorder. Nat. Biotechnol. 19: 805-806.
21. 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., et al. 2001. Intrinsically disordered protein. J. Mol. Graph. Model. 19: 26-59.
22. Dyson, H.J. and Wright, P.E. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6: 197-208.
23. Fearns, R. and Collins, P.L. 1999. Role of the M2-1 transcription antitermination protein of respiratory syncytial virus in sequential transcription. J. Virol. 73: 5852-5864.
24. Fletcher, C.M., McGuire, A.M., Gingras, A.C., Li, H., Matsuo, H., Sonenberg, N., and Wagner, G. 1998. 4E binding proteins inhibit the translation factor eIF4E without folded structure. Biochemistry 37: 9-15.
25. Fuxreiter, M., Simon, I., Friedrich, P., and Tompa, P. 2004. Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J. Mol. Biol. 338: 1015-1026.
26. Giraudon, P., Jacquier, M.F., and Wild, T.F. 1988. 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. 10: 137-152.
27. Guinier, A. and Fournet, F. 1955. Small angle scattering of X-rays. Wiley-Interscience, New York.
28. Hartlieb, B., Modrof, J., Muhlberger, E., Klenk, H.D., and Becker, S. 2003. Oligomerization of Ebola virus VP30 is essential for viral transcription and can be inhibited by a synthetic peptide. J. Biol. Chem. 278: 41830-41836.
29. Harty, R.N. and Palese, P. 1995. 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. 76: 2863-2867.
30. Heggeness, M.H., Scheid, A., and Choppin, P.W. 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. 77: 2631-2635.
31. _. 1981. The relationship of conformational changes in the Sendai virus nucleocapsid to proteolytic cleavage of the NP polypeptide. Virology 114: 555-562.
32. Hua, Q.X., Jia, W.H., Bullock, B.P., Habener, J.F., and Weiss, M.A. 1998. Transcriptional activator-coactivator recognition: Nascent folding of a kinase-inducible transactivation domain predicts its structure on coactivator binding. Biochemistry 37: 5858-5866.
33. Johansson, K., Bourhis, J.M., Campanacci, V., Cambillau, C., Canard, B., and Longhi, S. 2003. Crystal structure of the measles virus phosphoprotein domain responsible for the induced folding of the C-terminal domain of the nucleoprotein. J. Biol. Chem. 278: 44567-44573.
34. Karlin, D., Longhi, S., and Canard, B. 2002a. Substitution of two residues in the measles virus nucleoprotein results in an impaired self-association. Virology 302: 420-432.
35. Karlin, D., Longhi, S., Receveur, V., and Canard, B. 2002b. The N-terminal domain of the phosphoprotein of morbilliviruses belongs to the natively unfolded class of proteins. Virology 296: 251-262.
36. Karlin, D., Ferron, F., Canard, B., and Longhi, S. 2003. Structural disorder and modular organization in Paramyxovirinae N and P. J. Gen. Virol. 84: 3239-3252.
37. Kingston, R.L., Hamel, D.J., Gay, L.S., Dahlquist, F.W., and Matthews, B.W. 2004a. Structural basis for the attachment of a paramyxoviral polymerase to its template. Proc. Natl. Acad. Sci. 101: 8301-8306.
38. Kingston, R.L., Walter, A.B., and Gay, L.S. 2004b. Characterization of nucleocapsid binding by the measles and the mumps virus phosphoprotein. J. Virol. 78: 8615-8629.
39. Kozin, M.B. and Svergun, D.I. 2001. Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr. 34: 33-41.
40. Lacy, E.R., Filippov, I., Lewis, W.S., Otieno, S., Xiao, L., Weiss, S., Hengst, L., and Kriwacki, R.W. 2004. p27 binds cyclin-CDK complexes through a sequential mechanism involving binding-induced protein folding. Nat. Struct. Mol. Biol. 11: 358-364.
41. Laine, D., Trescol-Biémont, M., Longhi, S., Libeau, G., Marie, J., Vidalain, P., Azocar, O., Diallo, A., Canard, B., Rabourdin-Combe, C., 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.
42. Laine, D., Bourhis, J., Longhi, S., Flacher, M., Cassard, L., Canard, B., Sautès-Fridman, C., Rabourdin-Combe, C., and Valentin, H. 2005. Measles virus nucleoprotein induces cell proliferation arrest and apoptosis through NTAIL/NR and NCORE/FcgRIIB1 interactions, respectively. J. Gen. Virol. 86: 1771-1784.
43. Lamb, R.A. and Kolakofsky, D. 2001. Paramyxoviridae: The viruses and their replication. In Fields virology (eds. B.N. Fields, D.M. Knipe, and P.M. Howley), 4th ed., pp. 1305-1340. Lippincott-Raven, Philadelphia, PA.
44. Liston, P., DiFlumeri, C., and Briedis, D.J. 1995. Protein interactions entered into by the measles virus P, V, and C proteins. Virus Res. 38: 241-259.
45. Liston, P., Batal, R., DiFlumeri, C., and Briedis, D.J. 1997. Protein interaction domains of the measles virus nucleocapsid protein (NP). Arch. Virol. 142: 305-321.
46. Longhi, S., Receveur-Brechot, V., Karlin, D., Johansson, K., Darbon, H., Bhella, D., Yeo, R., Finet, S., and Canard, B. 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.
47. Marcotrigiano, J., Gingras, A.C., Sonenberg, N., and Burley, S.K. 1999. Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol. Cell 3: 707-716.
48. McGuffin, L.J., Bryson, K., and Jones, D.T. 2000. The PSIPRED protein structure prediction server. Bioinformatics 16: 404-405.
49. Mori, S., Abeygunawardana, C., Johnson, M.O., and van Zijl, P.C. 1995. Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. J. Magn. Reson. B 108: 94-98.
50. Morris, M.C., Mery, J., Heitz, A., Heitz, F., and Divita, G. 1999. Design and synthesis of a peptide derived from positions 195-244 of human cdc25C phosphatase. J. Peptide Sci. 5: 263-271.
51. Moyer, S.A., Baker, S.C., and Horikami, S.M. 1990. Host cell proteins required for measles virus reproduction. J. Gen. Virol. 71: 775-783.
52. Myers, J.K., Pace, C.N., and Scholtz, J.M. 1997a. Helix propensities are identical in proteins and peptides. Biochemistry 36: 10923-10929.
53. Myers, T.M., Pieters, A., and Moyer, S.A. 1997b. A highly conserved region of the Sendai virus nucleocapsid protein contributes to the NP-NP binding domain. Virology 229: 322-335.
54. Myers, T.M., Smallwood, S., and Moyer, S.A. 1999. Identification of nucleocapsid protein residues required for Sendai virus nucleocapsid formation and genome replication. J. Gen. Virol. 80: 1383-1391.
55. Narayanan, T., Diat, O., and Boesecke, P. 2001. SAXS and USAXS on the high brilliance beamline at the ESRF. Nucl. Instr. Methods Phys. Res. A 467: 1005-1009.
56. Oglesbee, M., Tatalick, L., Rice, J., and Krakowka, S. 1989. Isolation and characterization of canine distemper virus nucleocapsid variants. J. Gen. Virol. 70: 2409-2419.
57. Permyakov, S.E., Millett, I.S., Doniach, S., Permyakov, E.A., and Uversky, V.N. 2003. Natively unfolded C-terminal domain of caldesmon remains substantially unstructured after the effective binding to calmodulin. Proteins 53: 855-862.
58. Piotto, M., Saudek, V., and Sklenar, V. 1992. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2: 661-665.
59. Radhakrishnan, I., Perez-Alvarado, G.C., Parker, D., Dyson, H.J., Montminy, M.R., and Wright, P.E. 1997. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: A model for activator:coactivator interactions. Cell 91: 741-752.
60. Raggett, E.M., Bainbridge, G., Evans, L.J., Cooper, A., and Lakey, J.H. 1998. Discovery of critical Tol A-binding residues in the bactericidal toxin colicin N: A biophysical approach. Mol. Microbiol. 28: 1335-1343.
61. Rahaman, A., Srinivasan, N., Shamala, N., and Shaila, M.S. 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.
62. Robbins, S.J. and Bussell, R.H. 1979. Structural phosphoproteins associated with purified measles virions and cytoplasmic nucleocapsids. Intervirology 12: 96-102.
63. Robbins, S.J., Bussell, R.H., and Rapp, F. 1980. Isolation and partial characterization of two forms of cytoplasmic nucleocapsids from measles virus-infected cells. J. Gen. Virol. 47: 301-310.
64. Rost, B. 1996. PHD: Predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol. 266: 525-539.
65. Smallwood, S., Ryan, K.W., and Moyer, S.A. 1994. Deletion analysis defines a carboxyl-proximal region of Sendai virus P protein that binds to the polymerase L protein. Virology 202: 154-163.
66. Stallcup, K.C., Wechsler, S.L., and Fields, B.N. 1979. Purification of measles virus and characterization of subviral components. J. Virol. 30: 166-176.
67. Svergun, D. 1992. Determination of the regularization parameters in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25: 495-503.
68. Svergun, D.I., Baraberato, C., and Koch, M.H. 1995. CRYSOL - A program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28: 768-773.
69. Svergun, D.I., Petoukhov, M.V., and Koch, M.H. 2001. Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80: 2946-2953.
70. Tarbouriech, N., Curran, J., Ruigrok, R.W., and Burmeister, W.P. 2000. Tetrameric coiled coil domain of Sendai virus phosphoprotein. Nat. Struct. Biol. 7: 777-781.
71. tenOever, B.R., Servant, M.J., Grandvaux, N., Lin, R., and Hiscott, J. 2002. Recognition of the measles virus nucleocapsid as a mechanism of IRF-3 activation. J. Virol. 76: 3659-3669.
72. Tompa, P. 2002. Intrinsically unstructured proteins. Trends Biochem. Sci. 27: 527-533.
73. Tuckis, J., Smallwood, S., Feller, J.A., and Moyer, S.A. 2002. The C-terminal 88 amino acids of the Sendai virus P protein have multiple functions separable by mutation. J. Virol. 76: 68-77.
74. Uversky, V.N. 1993. Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule. Biochemistry 32: 13288-13298.
75. _. 2002. Natively unfolded proteins: A point where biology waits for physics. Protein Sci. 11: 739-756.
76. Vincent, S., Tigaud, I., Schneider, H., Buchholz, C.J., Yanagi, Y., and Gerlier, D. 2002. 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. 76: 6121-6130.
77. Wright, P.E. and Dyson, H.J. 1999. Intrinsically unstructured proteins: Reassessing the protein structure-function paradigm. J. Mol. Biol. 293: 321-331.
78. Zhang, X., Glendening, C., Linke, H., Parks, C.L., Brooks, C., Udem, S.A., and Oglesbee, M. 2002. Identification and characterization of a regulatory domain on the carboxyl terminus of the measles virus nucleocapsid protein. J. Virol. 76: 8737-8746.
79. Zhang, X., Bourhis, J.M., Longhi, S., Carsillo, T., Buccellato, M., Morin, B., Canard, B., and Oglesbee, M. 2005. Hsp72 recognizes a P binding motif in the measles virus N protein C-terminus. Virology 337: 162-174.