Fine mapping and characterization of the L-polymerase-binding domain of the respiratory syncytial virus phosphoprotein

Journal of Virology

Volumn 89, Issue 8, 2015, Pages 4421-4433

  Sourimant, Julien ^a,c   Rameix Welti, Marie Anne ^a,c,d   Gaillard, Anne Laure ^a   Chevret, Didier ^b   Galloux, Marie ^a   Gault, Elyanne ^c,d   Eléouët, Jean François ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

^b UMR1319 MICALIS   (France)

^c LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^d HÔPITAL AMBROISE PARÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACULOVIRUS VECTOR; LARGE PROTEIN; RECOMBINANT PROTEIN; RNA DIRECTED RNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS PHOSPHOPROTEIN; DNA DIRECTED RNA POLYMERASE; MULTIPROTEIN COMPLEX; PHOSPHOPROTEIN;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; GENE MUTATION; HUMAN RESPIRATORY SYNCYTIAL VIRUS; MOLECULAR RECOGNITION ELEMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; CELL LINE; CHEMICAL PHENOMENA; DNA SEQUENCE; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; GENETICS; HUMAN; IMMUNOBLOTTING; IMMUNOPRECIPITATION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLASMID; PROTEIN ANALYSIS; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE;

RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

AMINO ACID MOTIFS; BASE SEQUENCE; CELL LINE; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; MUTAGENESIS, SITE-DIRECTED; PHOSPHOPROTEINS; PLASMIDS; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; SEQUENCE ANALYSIS, DNA;

EID: 84925436560     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03619-14     Document Type: Article

References (53)

1. Tregoning JS, Schwarze J. 2010. Respiratory viral infections in infants: causes, clinical symptoms, virology, and immunology. Clin Microbiol Rev 23:74-98. http://dx.doi.org/10.1128/CMR.00032-09.
2. Collins PL, Melero JA. 2011. Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res 162: 80-99. http://dx.doi.org/10.1016/j.virusres.2011.09.020.
3. Valarcher JF, Taylor G. 2007. Bovine respiratory syncytial virus infection. Vet Res 38:153-180. http://dx.doi.org/10.1051/vetres:2006053.
4. Loregian A, Marsden HS, Palu G. 2002. Protein-protein interactions as targets for antiviral chemotherapy. Rev Med Virol 12:239-262. http://dx.doi.org/10.1002/rmv.356.
5. Morin B, Kranzusch PJ, Rahmeh AA, Whelan SP. 2013. The polymerase of negative-stranded RNA viruses. Curr Opin Virol 3:103-110. http://dx.doi.org/10.1016/j.coviro.2013.03.008.
6. Collins PL, Hill MG, Camargo E, Grosfeld H, Chanock RM, Murphy BR. 1995. Production of infectious human respiratory syncytial virus from cloned cDNA confirms an essential role for the transcription elongation factor from the 5= proximal open reading frame of the M2 mRNA in gene expression and provides a capability for vaccine development. Proc Natl Acad Sci USA 92:11563-11567. http://dx.doi.org/10.1073/pnas.92.25.11563.
7. Fearns R, Collins PL. 1999. Role of the M2-1 transcription antitermination protein of respiratory syncytial virus in sequential transcription. J Virol 73:5852-5864. http://jvi.asm.org/content/73/7/5852.long.
8. Hardy RW, Wertz GW. 1998. The product of the respiratory syncytial virus M2 gene ORF1 enhances readthrough of intergenic junctions during viral transcription. J Virol 72:520-526. http://jvi.asm.org/content/72/1/5 20.long.
9. Lahaye X, Vidy A, Pomier C, Obiang L, Harper F, Gaudin Y, Blondel D. 2009. Functional characterization of Negri bodies (NBs) in rabies virusinfected cells: evidence that NBs are sites of viral transcription and replication. J Virol 83:7948-7958. http://dx.doi.org/10.1128/JVI.00554-09.
10. Heinrich BS, Cureton DK, Rahmeh AA, Whelan SP. 2010. Protein expression redirects vesicular stomatitis virus RNA synthesis to cytoplasmic inclusions. PLoS Pathog 6:e1000958. http://dx.doi.org/10.1371/journal.ppat.100 0958.
11. Tawar RG, Duquerroy S, Vonrhein C, Varela PF, Damier-Piolle L, Castagne N, MacLellan K, Bedouelle H, Bricogne G, Bhella D, Eléouët JF, Rey FA. 2009. Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326:1279-1283. http://dx.doi.org/10.1126/science.1177634.
12. Blondot ML, Dubosclard V, Fix J, Lassoued S, Aumont-Nicaise M, Bontems F, Eléouët JF, Sizun C. 2012. Structure and functional analysis of the RNA-and viral phosphoprotein-binding domain of respiratory syncytial virus M2-1 protein. PLoS Pathog 8:e1002734. http://dx.doi.org/10.1371/journal.ppat.1002734.
13. Tanner SJ, Ariza A, Richard CA, Kyle HF, Dods RL, Blondot ML, Wu W, Trincao J, Trinh CH, Hiscox JA, Carroll MW, Silman NJ, Eléouët JF, Edwards TA, Barr JN. 2014. Crystal structure of the essential transcription antiterminator M2-1 protein of human respiratory syncytial virus and implications of its phosphorylation. Proc Natl Acad Sci U S A 111:1580-1585. http://dx.doi.org/10.1073/pnas.1317262111.
14. Leyrat C, Renner M, Harlos K, Grimes JM. 2013. Solution and crystallographic structures of the central region of the phosphoprotein from human metapneumovirus. PLoS One 8:e80371. http://dx.doi.org/10.1371/journal.pone.0080371.
15. Castagné N, Barbier A, Bernard J, Rezaei H, Huet JC, Henry C, Da Costa B, Eléouët JF. 2004. Biochemical characterization of the respiratory syncytial virus P-P and P-N protein complexes and localization of the P protein oligomerization domain. J Gen Virol 85:1643-1653. http://dx.doi.org/10.1099/vir.0.79830-0.
16. Ruigrok RW, Crepin T. 2010. Nucleoproteins of negative strand RNA viruses; RNA binding, oligomerisation and binding to polymerase cofactor. Viruses 2:27-32. http://dx.doi.org/10.3390/v2010027.
17. Navarro J, Lopez-Otin C, Villanueva N. 1991. Location of phosphorylated residues in human respiratory syncytial virus phosphoprotein. J Gen Virol 72(Part 6):1455-1459. http://dx.doi.org/10.1099/0022-1317-72-6-1455.
18. Mazumder B, Barik S. 1994. Requirement of casein kinase II-mediated phosphorylation for the transcriptional activity of human respiratory syncytial viral phosphoprotein P: transdominant negative phenotype of phosphorylation-defective P mutants. Virology 205:104-111. http://dx.doi.org/10.1006/viro.1994.1624.
19. Mazumder B, Adhikary G, Barik S. 1994. Bacterial expression of human respiratory syncytial viral phosphoprotein P and identification of Ser237 as the site of phosphorylation by cellular casein kinase II. Virology 205: 93-103. http://dx.doi.org/10.1006/viro.1994.1623.
20. Barik S, McLean T, Dupuy LC. 1995. Phosphorylation of Ser232 directly regulates the transcriptional activity of the P protein of human respiratory syncytial virus: phosphorylation of Ser237 may play an accessory role. Virology 213:405-412. http://dx.doi.org/10.1006/viro.1995.0013.
21. Dupuy LC, Dobson S, Bitko V, Barik S. 1999. Casein kinase 2-mediated phosphorylation of respiratory syncytial virus phosphoprotein P is essential for the transcription elongation activity of the viral polymerase; phosphorylation by casein kinase 1 occurs mainly at Ser215 and is without effect. J Virol 73:8384-8392. http://jvi.asm.org/content/73/10/8384.long.
22. Asenjo A, Villanueva N. 2000. Regulated but not constitutive human respiratory syncytial virus (HRSV) P protein phosphorylation is essential for oligomerization. FEBS Lett 467:279-284. http://dx.doi.org/10.1016/S0014-5793(00)01171-6.
23. Villanueva N, Hardy R, Asenjo A, Yu Q, Wertz G. 2000. The bulk of the phosphorylation of human respiratory syncytial virus phosphoprotein is not essential but modulates viral RNA transcription and replication. J Gen Virol 81:129-133. http://vir.sgmjournals.org/content/81/1/129.long.
24. Lu B, Ma CH, Brazas R, Jin H. 2002. The major phosphorylation sites of the respiratory syncytial virus phosphoprotein are dispensable for virus replication in vitro. J Virol 76:10776-10784. http://dx.doi.org/10.1128/JVI.76.21.10776-10784.2002.
25. Asenjo A, Rodriguez L, Villanueva N. 2005. Determination of phosphorylated residues from human respiratory syncytial virus P protein that are dynamically dephosphorylated by cellular phosphatases: a possible role for serine 54. J Gen Virol 86:1109-1120. http://dx.doi.org/10.1099/vir.0.80692-0.
26. Asenjo A, Calvo E, Villanueva N. 2006. Phosphorylation of human respiratory syncytial virus P protein at threonine 108 controls its interaction with the M2-1 protein in the viral RNA polymerase complex. J Gen Virol 87:3637-3642. http://dx.doi.org/10.1099/vir.0.82165-0.
27. Llorente MT, Garcia-Barreno B, Calero M, Camafeita E, Lopez JA, Longhi S, Ferron F, Varela PF, Melero JA. 2006. Structural analysis of the human respiratory syncytial virus phosphoprotein: characterization of an alpha-helical domain involved in oligomerization. J Gen Virol 87:159-169. http://dx.doi.org/10.1099/vir.0.81430-0.
28. Esperante SA, Paris G, de Prat-Gay G. 2012. Modular unfolding and dissociation of the human respiratory syncytial virus phosphoprotein P and its interaction with the M(2-1) antiterminator: a singular tetramertetramer interface arrangement. Biochemistry 51:8100-8110. http://dx.doi.org/10.1021/bi300765c.
29. Simabuco FM, Asara JM, Guerrero MC, Libermann TA, Zerbini LF, Ventura AM. 2011. Structural analysis of human respiratory syncytial virus P protein: identification of intrinsically disordered domains. Braz J Microbiol 42:340-345. http://dx.doi.org/10.1590/S1517-83822011000100043.
30. Slack MS, Easton AJ. 1998. Characterization of the interaction of the human respiratory syncytial virus phosphoprotein and nucleocapsid protein using the two-hybrid system. Virus Res 55:167-176. http://dx.doi.org/10.1016/S0168-1702(98)00042-2.
31. Tran TL, Castagne N, Bhella D, Varela PF, Bernard J, Chilmonczyk S, Berkenkamp S, Benhamo V, Grznarova K, Grosclaude J, Nespoulos C, Rey FA, Eléouët JF. 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. http://dx.doi.org/10.1099/vir.0.82282-0.
32. Khattar SK, Yunus AS, Samal SK. 2001. Mapping the domains on the phosphoprotein of bovine respiratory syncytial virus required for N-P and P-L interactions using a minigenome system. J Gen Virol 82:775-779. http://vir.sgmjournals.org/content/82/4/775.long.
33. Byrappa S, Gavin DK, Gupta KC. 1995. A highly efficient procedure for site-specific mutagenesis of full-length plasmids using Vent DNA polymerase. Genome Res 5:404-407. http://dx.doi.org/10.1101/gr.5.4.404.
34. Fix J, Galloux M, Blondot ML, Eléouët JF. 2011. The insertion of fluorescent proteins in a variable region of respiratory syncytial virus L polymerase results in fluorescent and functional enzymes but with reduced activities. Open Virol J 5:103-108. http://dx.doi.org/10.2174/1874357901105010103.
35. Buchholz UJ, Finke S, Conzelmann KK. 1999. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73:251-259. http://jvi.asm.org/content/73/1/251.long.
36. Yu Q, Hardy RW, Wertz GW. 1995. Functional cDNA clones of the human respiratory syncytial (RS) virus N, P, and L proteins support replication of RS virus genomicRNAanalogs and define minimal trans-acting requirements for RNA replication. J Virol 69:2412-2419. http://jvi.asm.org/content/69/4/2412.long.
37. Tran TL, Castagné N, Dubosclard V, Noinville S, Koch E, Moudjou M, Henry C, Bernard J, Yeo RP, Eléouët JF. 2009. The respiratory syncytial virus M2-1 protein forms tetramers and interacts with RNA and P in a competitive manner. J Virol 83:6363-6374. http://dx.doi.org/10.1128/JVI.00335-09.
38. Sutter G, Ohlmann M, Erfle V. 1995. Non-replicating vaccinia vector efficiently expresses bacteriophage T7 RNA polymerase. FEBS Lett 371:9-12. http://dx.doi.org/10.1016/0014-5793(95)00843-X.
39. Wyatt LS, Moss B, Rozenblatt S. 1995. Replication-deficient vaccinia virus encoding bacteriophage T7 RNA polymerase for transient gene expression in mammalian cells. Virology 210:202-205. http://dx.doi.org/10.1006/viro.1995.1332.
40. Noton SL, Deflube LR, Tremaglio CZ, Fearns R. 2012. The respiratory syncytial virus polymerase has multiple RNA synthesis activities at the promoter. PLoS Pathog 8:e1002980. http://dx.doi.org/10.1371/journal.ppat.1002980.
41. Galloux M, Tarus B, Blazevic I, Fix J, Duquerroy S, Eléouët JF. 2012. Characterization of a viral phosphoprotein binding site on the surface of the respiratory syncytial nucleoprotein. J Virol 86:8375-8387. http://dx.doi.org/10.1128/JVI.00058-12.
42. García J, Garcia-Barreno B, Vivo A, Melero JA. 1993. Cytoplasmic inclusions of respiratory syncytial virus-infected cells: formation of inclusion bodies in transfected cells that coexpress the nucleoprotein, the phosphoprotein, and the 22K protein. Virology 195:243-247. http://dx.doi.org/10.1006/viro.1993.1366.
43. Morin B, Rahmeh AA, Whelan SP. 2012. Mechanism of RNA synthesis initiation by the vesicular stomatitis virus polymerase. EMBO J 31:1320-1329. http://dx.doi.org/10.1038/emboj.2011.483.
44. Grosfeld H, Hill MG, Collins PL. 1995. RNA replication by respiratory syncytial virus (RSV) is directed by the N, P, and L proteins; transcription also occurs under these conditions but requires RSV superinfection for efficient synthesis of full-length mRNA. J Virol 69:5677-5686. http://jvi.asm.org/content/69/9/5677.long.
45. Cox R, Pickar A, Qiu S, Tsao J, Rodenburg C, Dokland T, Elson A, He B, Luo M. 2014. Structural studies on the authentic mumps virus nucleocapsid showing uncoiling by the phosphoprotein. Proc Natl Acad Sci U S A 111:15208-15213. http://dx.doi.org/10.1073/pnas.1413268111.
46. 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. http://dx.doi.org/10.1016/j.virol.2008.10.019.
47. Asenjo A, Mendieta J, Gomez-Puertas P, Villanueva N. 2008. Residues in human respiratory syncytial virus P protein that are essential for its activity on RNA viral synthesis. Virus Res 132:160-173. http://dx.doi.org/10.1016/j.virusres.2007.11.013.
48. Smallwood S, Ryan KW, Moyer SA. 1994. Deletion analysis defines a carboxyl-proximal region of Sendai virus P protein that binds to the polymerase L protein. Virology 202:154-163. http://dx.doi.org/10.1006/viro.1994.1331.
49. Tarbouriech N, Curran J, Ruigrok RW, Burmeister WP. 2000. Tetrameric coiled coil domain of Sendai virus phosphoprotein. Nat Struct Biol 7:777-781. http://dx.doi.org/10.1038/79013.
50. Chenik M, Schnell M, Conzelmann KK, Blondel D. 1998. Mapping the interacting domains between the rabies virus polymerase and phosphoprotein. J Virol 72:1925-1930. http://jvi.asm.org/content/72/3/1925.long.
51. Emerson SU, Schubert M. 1987. Location of the binding domains for the RNA polymerase L and the ribonucleocapsid template within different halves of the NS phosphoprotein of vesicular stomatitis virus. Proc Natl Acad Sci U S A 84:5655-5659. http://dx.doi.org/10.1073/pnas.84.16.5655.
52. Rahmeh AA, Morin B, Schenk AD, Liang B, Heinrich BS, Brusic V, Walz T, Whelan SP. 2012. Critical phosphoprotein elements that regulate polymerase architecture and function in vesicular stomatitis virus. Proc Natl Acad Sci U S A 109:14628-14633. http://dx.doi.org/10.1073/pnas.1209147109.
53. Llorente MT, Taylor IA, Lopez-Vinas E, Gomez-Puertas P, Calder LJ, Garcia-Barreno B, Melero JA. 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. http://dx.doi.org/10.1002/prot.21988.