Insights into the coiled-coil organization of the Hendra virus phosphoprotein from combined biochemical and SAXS studies

Virology

Volumn 477, Issue , 2015, Pages 42-55

  Beltrandi, Matilde ^a,b   Blocquel, David ^a,b   Erales, Jenny ^a,b   Barbier, Pascale ^c   Cavalli, Andrea ^d,e   Longhi, Sonia ^a,b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b CNRS   (France)

^c University of the Mediterranean Aix Marseille II   (France)

^d INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Coiled coil; Cross linking; Hendra virus; Henipavirus; Homotrimer; P multimerization domain; Phosphoprotein; PMD; Small angle X ray scattering

Indexed keywords

VIRUS PHOSPHOPROTEIN; PHOSPHOPROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HENDRA VIRUS; MOLECULAR CLONING; NIPAH VIRUS; NONHUMAN; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; ULTRACENTRIFUGATION; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SMALL ANGLE SCATTERING;

HENDRA VIRUS; HENIPAVIRUS; NIPAH VIRUS;

HENDRA VIRUS; PHOSPHOPROTEINS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SCATTERING, SMALL ANGLE; ULTRACENTRIFUGATION;

EID: 84921960964     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.12.029     Document Type: Article

References (63)

1. 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.
2. Blocquel D., Beltrandi M., Erales J., Barbier P., Longhi S. Biochemical and structural studies of the oligomerization domain of the Nipah virus phosphoprotein: evidence for an elongated coiled-coil homotrimer. Virology 2013, 446:162-172.
3. Blocquel D., Bourhis J.M., Eléouët J.F., Gerlier D., Habchi J., Jamin M., Longhi S., Yabukarski F. Transcription et réplication des Mononégavirales: une machine moléculaire originale. Virologie 2012, 16:225-257.
4. Blocquel D., Habchi J., Durand E., Sevajol M., Ferron F., Erales J., Papageorgiou N., Longhi S. Coiled-coil deformations in crystal structures: the measles virus phosphoprotein multimerization domain as an illustrative example. Acta Cryst. D 2014, 70:1589-1603.
5. Blocquel D., Habchi J., Gruet A., Blangy S., Longhi S. Compaction and binding properties of the intrinsically disordered C-terminal domain of Henipavirus nucleoprotein as unveiled by deletion studies. Mol. Biosyst. 2012, 8:392-410.
6. Bruhn-Johannsen J.F., Barnett K., Bibby J., Thomas J., Keegan R., Rigden D., Bornholdt Z.A., Saphire E.O. Crystal structure of the Nipah virus phosphoprotein tetramerization domain. J. Virol. 2014, 88:758-762.
7. Chan Y.P., Koh C.L., Lam S.K., Wang L.F. Mapping of domains responsible for nucleocapsid protein-phosphoprotein interaction of Henipaviruses. J. Gen. Virol. 2004, 85:1675-1684.
8. Chouard T. Structural biology: breaking the protein rules. Nature 2011, 471:151-153.
9. Communie G., Crepin T., Maurin D., Jensen M.R., Blackledge M., Ruigrok R.W. Structure of the tetramerization domain of measles virus phosphoprotein. J. Virol. 2013, 87:7166-7169.
10. Communie G., Habchi J., Yabukarski F., Blocquel D., Schneider R., Tarbouriech N., Papageorgiou N., Ruigrok R.W., Jamin M., Ringkjøbing-Jensen M., Longhi S., Blackledge M. Atomic resolution description of the interaction between the nucleoprotein and phosphoprotein of Hendra virus. PLoS Pathog. 2013, 9:e1003631.
11. Cox R., Green T.J., Purushotham S., Deivanayagam C., Bedwell G.J., Prevelige P.E., Luo M. Structural and functional characterization of the mumps virus phosphoprotein. J. Virol. 2013, 87:7558-7568.
12. Curran J. A role for the Sendai virus P protein trimer in RNA synthesis. J. Virol. 1998, 72:4274-4280.
13. Curran J., Boeck R., Lin-Marq N., Lupas A., Kolakofsky D. Paramyxovirus phosphoproteins form homotrimers as determined by an epitope dilution assay, via predicted coiled coils. Virology 1995, 214:139-149.
14. DeLano W.L. The PyMOL molecular graphics system. Proteins: Struct., Funct. Bioinform. 2002, 30:442-454.
15. Dunker A.K., Oldfield C.J., Meng J., Romero P., Yang J.Y., Chen J.W., Vacic V., Obradovic Z., Uversky V.N. The unfoldomics decade: an update on intrinsically disordered proteins. BMC Genomics 2008, 9(Suppl. 2):S1.
16. Dunker A.K., Silman I., Uversky V.N., Sussman J.L. Function and structure of inherently disordered proteins. Curr. Opin. Struct. Biol. 2008, 18:756-764.
17. Dutta K., Alexandrov A., Huang H., Pascal S.M. pH-induced folding of an apoptotic coiled coil. Protein Sci. 2001, 10:2531-2540.
18. Eaton B.T., Mackenzie J.S., Wang L.F. Henipaviruses. Fields Virology 2007, 1587-1600. Lippincott-Raven, Philadelphia. 5th ed. B.N. Fields, D.M. Knipe, P.M. Howley (Eds.).
19. Ferron F., Rancurel C., Longhi S., Cambillau C., Henrissat B., Canard B. VaZyMolO: a tool to define and classify modularity in viral proteins. J. Gen. Virol. 2005, 86:743-749.
20. Forster F., Webb B., Krukenberg K.A., Tsuruta H., Agard D.A., Sali A. Integration of small-angle X-ray scattering data into structural modeling of proteins and their assemblies. J. Mol. Biol. 2008, 382:1089-1106.
21. Franke D., Svergun D.I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Cryst. 2009, 42:342-346.
22. Fu B., Sahakyan A.B., Camilloni C., Tartaglia G.G., Paci E., Caflisch A., Vendruscolo M., Cavalli A. ALMOST: an all atom molecular simulation toolkit for protein structure determination. J. Comput. Chem. 2014, 35:1101-1105.
23. Habchi J., Blangy S., Mamelli L., Ringkjobing Jensen M., Blackledge M., Darbon H., Oglesbee M., Shu Y., Longhi S. Characterization of the interactions between the nucleoprotein and the phosphoprotein of Henipaviruses. J. Biol. Chem. 2011, 286:13583-13602.
24. Habchi J., Mamelli L., Darbon H., Longhi S. Structural disorder within Henipavirus nucleoprotein and phosphoprotein: from predictions to experimental assessment. PLoS ONE 2010, 5:e11684.
25. Habchi J., Tompa P., Longhi S., Uversky V.N. Introducing protein intrinsic disorder. Chem. Rev. 2014, 114:6561-6588.
26. 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.
27. Karplus K., Karchin R., Draper J., Casper J., Mandel-Gutfreund Y., Diekhans M., Hughey R. Combining local-structure, fold-recognition, and new fold methods for protein structure prediction. Proteins 2003, 53(Suppl. 6):S491-S496.
28. Karplus K., Katzman S., Shackleford G., Koeva M., Draper J., Barnes B., Soriano M., Hughey R. SAM-T04: what is new in protein-structure prediction for CASP6. Proteins 2005, 61(Suppl. 7):S135-S142.
29. Kass R., Raftery A. Bayes factors. J. Am. Stat. Assoc. 1995, 90:773-795.
30. Katzman S., Barrett C., Thiltgen G., Karchin R., Karplus K. PREDICT-2ND: a tool for generalized protein local structure prediction. Bioinformatics 2008, 24:2453-2459.
31. Konarev P.V., Volkov V.V., Sokolova A.V., Koch M.H.J., Svergun D.I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Cryst. 2003, 36:1277-1282.
32. Lamb R.A., Parks G.D. Paramyxoviridae: the viruses and their replication. Fields Virology 2007, 1450-1497. Lippincott Williams & Wilkins, Philadelphia, PA. 5th edition. D.M. Knipe, P.M. Howley (Eds.).
33. Lau S.Y., Taneja A.K., Hodges R.S. Synthesis of a model protein of defined secondary and quaternary structure. Effect of chain length on the stabilization and formation of two-stranded alpha-helical coiled-coils. J. Biol. Chem. 1984, 259:13253-13261.
34. Laue T.M., Shah B.D., Ridgeway T.M., Pelletier S.L. Computer-aided interpretation of analytical sedimentation data for proteins in analytical ultracentrifugation 1992, 90-125. Biochemistry and Polymer Sciences Royal Society of Chemistry, Cambridge, UK. S.E. Harding, A.J. Rowe, J.C. Horton (Eds.).
35. Lazaridis T., Karplus M. Effective energy function for proteins in solution. Proteins 1999, 35:133-152.
36. 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.
37. Llorente M.T., Taylor I.A., Lopez-Vinas E., Gomez-Puertas P., Calder L.J., Garcia-Barreno B., Melero J.A. 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 2008, 72:946-958.
38. Lupas A.N., Gruber M. The structure of alpha-helical coiled coils. Adv. Protein Chem. 2005, 70:37-78.
39. Marsh G.A., de Jong C., Barr J.A., Tachedjian M., Smith C., Middleton D., Yu M., Todd S., Foord A.J., Haring V., Payne J., Robinson R., Broz I., Crameri G., Field H.E., Wang L.F. Cedar virus: a novel Henipavirus isolated from Australian bats. PLoS Pathog. 2012, 8:e1002836.
40. Mylonas E., Svergun D. Accuracy of molecular mass determination of proteins in solution by small-angle X-ray scattering. J. Appl. Crystallogr. 2007, 40:s245-s249.
41. Omi-Furutani M., Yoneda M., Fujita K., Ikeda F., Kai C. Novel phosphoprotein-interacting region in Nipah virus nucleocapsid protein and its involvement in viral replication. J. Virol. 2010, 84:9793-9799.
42. Oshaben K.M., Salari R., McCaslin D.R., Chong L.T., Horne W.S. The native GCN4 leucine-zipper domain does not uniquely specify a dimeric oligomerization state. Biochemistry 2012, 51:9581-9591.
43. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
44. 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.
45. Rambo R.P., Tainer J.A. Accurate assessment of mass, models and resolution by small-angle scattering. Nature 2013, 496:477-481.
46. Roux L. Dans le génome des Paramyxovirinae, les promoteurs et leurs activités sont façonnés par la≪règle de six. Virologie 2005, 9:19-34.
47. Salvamani S., Goh Z., Ho K., Tey B., Tan W. Oligomerization state of the multimerization domain of Nipah virus phosphoprotein. Process Biochem. 2013, 48:1476-1480.
48. Svergun D. Determination of the regularization parameters in indirect-trasform methods using perceptual criteria. J. Appl. Cryst. 1992, 25:495-503.
49. Svergun D., Barberato C., Koch M.H.J. CRYSOL, a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Cryst. 1995, 28:768-773.
50. 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.
51. 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.
52. Turoverov K.K., Kuznetsova I.M., Uversky V.N. The protein kingdom extended: ordered and intrinsically disordered proteins, their folding, supramolecular complex formation, and aggregation. Prog. Biophys. Mol. Biol. 2010, 102:73-84.
53. Uversky V.N. What does it mean to be natively unfolded?. Eur. J. Biochem. 2002, 269:2-12.
54. Uversky V.N. The mysterious unfoldome: structureless, underappreciated, yet vital part of any given proteome. J. Biomed. Biotechnol. 2010, 2010:568068.
55. Uversky, V.N., 2013. A decade and a half of protein intrinsic disorder: Biology still waits for physics. Protein Sci.
56. Uversky V.N., Dunker A.K. Understanding protein non-folding. Biochim. Biophys. Acta 2010, 1804:1231-1264.
57. Vistica J., Dam J., Balbo A., Yikilmaz E., Mariuzza R.A., Rouault T.A., Schuck P. Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal. Biochem. 2004, 326:234-256.
58. Volkov V.V., Svergun D.I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Cryst. 2003, 36:860-864.
59. Wang L.F., Yu M., Hansson E., Pritchard L.I., Shiell B., Michalski W.P., Eaton B.T. The exceptionally large genome of Hendra virus: support for creation of a new genus within the family Paramyxoviridae. J. Virol. 2000, 74:9972-9979.
60. Whitmore L., Wallace B.A. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 2004, 32:W668-W673.
61. Whitmore L., Wallace B.A. Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 2008, 89:392-400.
62. Wilkins D.K., Grimshaw S.B., Receveur V., Dobson C.M., Jones J.A., Smith L.J. Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 1999, 38:16424-16431.
63. Woody R.W. Circular dichroism of intrinsically disordered proteins. Instrumental Analysis of Intrinsically Disordered Proteins: Assessing Structure and Conformation 2010, 303-321. John Wiley and Sons, Hoboken (NJ). V.N. Uversky, S. Longhi (Eds.).