Interactome analysis of the human respiratory syncytial virus RNA polymerase complex identifies protein chaperones as important cofactors that promote L-protein stability and RNA synthesis

Journal of Virology

Volumn 89, Issue 2, 2015, Pages 917-930

  Munday, Diane C ^a   Wu, Weining ^a   Smith, Nikki ^b   Fix, Jenna ^c   Noton, Sarah Louise ^d   Galloux, Marie ^c   Touzelet, Olivier ^a   Armstrong, Stuart D ^a   Dawson, Jenna M ^a   Aljabr, Waleed ^a   Easton, Andrew J ^e   Rameix Welti, Marie Anne ^c   de Oliveira, Andressa Peres ^f   Simabuco, Fernando M ^g   Ventura, Armando M ^f   Hughes, David J ^h   Barr, John N ^h   Fearns, Rachel ^d   Digard, Paul ^b   Eléouët, Jean François ^c   Hiscox, Julian A ^a,i   more..

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

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

^d BOSTON UNIVERSITY   (United States)

^e UNIVERSITY OF WARWICK   (United Kingdom)

^f UNIVERSITY OF SÃO PAULO   (Brazil)

^g UNIVERSITY OF CAMPINAS   (Brazil)

^h UNIVERSITY OF LEEDS   (United Kingdom)

ⁱ NIHR Health Protections Research Unit in Emerging and Zoonotic Infections   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; ENHANCED GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 90; RNA POLYMERASE; DNA DIRECTED RNA POLYMERASE; HEAT SHOCK PROTEIN 70; PROTEIN BINDING; VIRUS PROTEIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOPRECIPITATION; NONHUMAN; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RNA SYNTHESIS; VIRUS GENE; VIRUS REPLICATION; VIRUS TITRATION; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS;

HUMAN RESPIRATORY SYNCYTIAL VIRUS; HYDRANGEA RINGSPOT VIRUS; MAMMALIA;

DNA-DIRECTED RNA POLYMERASES; HOST-PATHOGEN INTERACTIONS; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; PROTEIN STABILITY; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84920842335     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01783-14     Document Type: Article

References (49)

1. 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.
2. Nokes JD, Cane PA. 2008. New strategies for control of respiratory syncytial virus infection. Curr Opin Infect Dis 21:639-643. http://dx.doi.org/10.1097/QCO.0b013e3283184245.
3. Collins PL, Graham BS. 2008. Viral and host factors in human respiratory syncytial virus pathogenesis. J Virol 82:2040-2055. http://dx.doi.org/10.1128/JVI.01625-07.
4. Tawar RG, Duquerroy S, Vonrhein C, Varela PF, Damier-Piolle L, Castagne N, MacLellan K, Bedouelle H, Bricogne G, Bhella D, Eleouet 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.
5. Fearns R, Collins PL. 1999. Role of the M2-1 transcription antitermina-tion protein of respiratory syncytial virus in sequential transcription. J Virol 73:5852-5864.
6. Galloux M, Tarus B, Blazevic I, Fix J, Duquerroy S, Eleouet 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.
7. Wileman T. 2006. Aggresomes and autophagy generate sites for virus replication. Science 312:875-878. http://dx.doi.org/10.1126/science.1126766.
8. Kirkegaard K. 2009. Subversion of the cellular autophagy pathway by viruses. Curr Top Microbiol Immunol 335:323-333. http://dx.doi.org/10.1007/978-3-642-00302-8_16.
9. Kidmose RT, Vasiliev NN, Chetverin AB, Andersen GR, Knudsen CR. 2010. Structure of the Qβ replicase, an RNA-dependent RNA polymerase consisting of viral and host proteins. Proc Natl Acad Sci USA 107:10884-10889. http://dx.doi.org/10.1073/pnas.1003015107.
10. Nagata K, Kawaguchi A, Naito T. 2008. Host factors for replication and transcription of the influenza virus genome. Rev Med Virol 18:247-260. http://dx.doi.org/10.1002/rmv.575.
11. 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.
12. Oliveira AP, Simabuco FM, Tamura RE, Guerrero MC, Ribeiro PG, Libermann TA, Zerbini LF, Ventura AM. 2013. Human respiratory syncytial virus N, P and M protein interactions in HEK-293T cells. Virus Res 177:108-112. http://dx.doi.org/10.1016/j.virusres.2013.07.010.
13. Brown G, Rixon HW, Steel J, McDonald TP, Pitt AR, Graham S, Sugrue RJ. 2005. Evidence for an association between heat shock protein 70 and the respiratory syncytial virus polymerase complex within lipid-raft membranes during virus infection. Virology 338:69-80. http://dx.doi.org/10.1016/j.virol.2005.05.004.
14. Radhakrishnan A, Yeo D, Brown G, Myaing MZ, Iyer LR, Fleck R, Tan BH, Aitken J, Sanmun D, Tang K, Yarwood A, Brink J, Sugrue RJ. 2010. Protein analysis of purified respiratory syncytial virus particles reveals an important role for heat shock protein 90 in virus particle assembly. Mol Cell Proteomics 9:1829-1848. http://dx.doi.org/10.1074/mcp.M110.001651.
15. Geller R, Andino R, Frydman J. 2013. Hsp90 inhibitors exhibit resistance-free antiviral activity against respiratory syncytial virus. PLoS One 8:e56762. http://dx.doi.org/10.1371/journal.pone.0056762.
16. Connor JH, McKenzie MO, Parks GD, Lyles DS. 2007. Antiviral activity and RNA polymerase degradation following Hsp90 inhibition in a range of negative strand viruses. Virology 362:109-119. http://dx.doi.org/10.1016/j.virol.2006.12.026.
17. Fix J, Galloux M, Blondot ML, Eleouet 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.
18. Wu W, Tran KC, Teng MN, Heesom KJ, Matthews DA, Barr JN, Hiscox JA. 2012. The interactome of the human respiratory syncytial virus NS1 protein highlights multiple effects on host cell biology. J Virol 86:7777-7789. http://dx.doi.org/10.1128/JVI.00460-12.
19. Jourdan SS, Osorio F, Hiscox JA. 2012. An interactome map of the nucleocapsid protein from a highly pathogenic North American porcine reproductive and respiratory syndrome virus strain generated using SILAC-based quantitative proteomics. Proteomics 12:1015-1023. http://dx.doi.org/10.1002/pmic.201100469.
20. Emmott E, Munday D, Bickerton E, Britton P, Rodgers MA, Whitehouse A, Zhou EM, Hiscox JA. 2013. The cellular interactome of the coronavirus infectious bronchitis virus nucleocapsid protein and functional implications for virus biology. J Virol 87:9486-9500. http://dx.doi.org/10.1128/JVI.00321-13.
21. Garcia-Dorival I, Wu W, Dowall S, Armstrong S, Touzelet O, Wastling J, Barr JN, Matthews D, Carroll M, Hewson R, Hiscox JA. 2014. Elucidation of the Ebola virus VP24 cellular interactome and disruption of virus biology through targeted inhibition of host cell protein function. J Proteome Res 13:5120-2135. http://dx.doi.org/10.1021/pr500556d.
22. Neckers L, Tatu U. 2008. Molecular chaperones in pathogen virulence: emerging new targets for therapy. Cell Host Microbe 4:519-527. http://dx.doi.org/10.1016/j.chom.2008.10.011.
23. Geller R, Taguwa S, Frydman J. 2012. Broad action of Hsp90 as a host chaperone required for viral replication. Biochim Biophys Acta 1823:698-706. http://dx.doi.org/10.1016/j.bbamcr.2011.11.007.
24. Ueba O. 1978. Respiratory syncytial virus. I. Concentration and purification of the infectious virus. Acta Med Okayama 32:265-272.
25. Munday DC, Emmott E, Surtees R, Lardeau CH, Wu W, Duprex WP, Dove BK, Barr JN, Hiscox JA. 2010. Quantitative proteomic analysis of A549 cells infected with human respiratory syncytial virus. Mol Cell Proteomics 9:2438-2459. http://dx.doi.org/10.1074/mcp.M110.001859.
26. Canter DM, Jackson RL, Perrault J. 1993. Faithful and efficient in vitro reconstitution of vesicular stomatitis virus transcription using plasmidencoded L and P proteins. Virology 194:518-529. http://dx.doi.org/10.1006/viro.1993.1290.
27. Desterro JM, Keegan LP, Lafarga M, Berciano MT, O'Connell M, Carmo-Fonseca M. 2003. Dynamic association of RNA-editing enzymes with the nucleolus. J Cell Sci 116:1805-1818. http://dx.doi.org/10.1242/jcs.00371.
28. Tanner SJ, Ariza A, Richard CA, Kyle HF, Dods RL, Blondot ML, Wu W, Trincao J, Trinh CH, Hiscox JA, Carroll MW, Silman NJ, Eleouet 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 USA 111:1580-1585. http://dx.doi.org/10.1073/pnas.1317262111.
29. Trinkle-Mulcahy L, Boulon S, Lam YW, Urcia R, Boisvert FM, Vandermoere F, Morrice NA, Swift S, Rothbauer U, Leonhardt H, Lamond A. 2008. Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. J Cell Biol 183:223-239. http://dx.doi.org/10.1083/jcb.200805092.
30. Boulon S, Ahmad Y, Trinkle-Mulcahy L, Verheggen C, Cobley A, Gregor P, Bertrand E, Whitehorn M, Lamond AI. 2010. Establishment of a protein frequency library and its application in the reliable identification of specific protein interaction partners. Mol Cell Proteomics 9:861-879. http://dx.doi.org/10.1074/mcp.M900517-MCP200.
31. 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.
32. Prevost M, Chamousset D, Nasa I, Freele E, Morrice N, Moorhead G, Trinkle-Mulcahy L. 2013. Quantitative fragmentome mapping reveals novel, domain-specific partners for the modular protein RepoMan (recruits PP1 onto mitotic chromatin at anaphase). Mol Cell Proteomics 12:1468-1486. http://dx.doi.org/10.1074/mcp.M112.023291.
33. De Wever V, Lloyd DC, Nasa I, Nimick M, Trinkle-Mulcahy L, Gourlay R, Morrice N, Moorhead GB. 2012. Isolation of human mitotic protein phosphatase complexes: identification of a complex between protein phosphatase 1 and the RNA helicase Ddx21. PLoS One 7:e39510. http://dx.doi.org/10.1371/journal.pone.0039510.
34. Garcia 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.
35. Tremaglio CZ, Noton SL, Deflube LR, Fearns R. 2013. Respiratory syncytial virus polymerase can initiate transcription from position 3 of the leader promoter. J Virol 87:3196-3207. http://dx.doi.org/10.1128/JVI.02862-12.
36. Liu S, Hao Q, Peng N, Yue X, Wang Y, Chen Y, Wu J, Zhu Y. 2012. Major vault protein: a virus-induced host factor against viral replication through the induction of type-I interferon. Hepatology 56:57-66. http://dx.doi.org/10.1002/hep.25642.
37. Burke E, Dupuy L, Wall C, Barik S. 1998. Role of cellular actin in the gene expression and morphogenesis of human respiratory syncytial virus. Virology 252:137-148. http://dx.doi.org/10.1006/viro.1998.9471.
38. Burke E, Mahoney NM, Almo SC, Barik S. 2000. Profilin is required for optimal actin-dependent transcription of respiratory syncytial virus genome RNA. J Virol 74:669-675. http://dx.doi.org/10.1128/JVI.74.2.669-675.2000.
39. Harpen M, Barik T, Musiyenko A, Barik S. 2009. Mutational analysis reveals a noncontractile but interactive role of actin and profilin in viral RNA-dependent RNA synthesis. J Virol 83:10869-10876. http://dx.doi.org/10.1128/JVI.01271-09.
40. Duprex WP, Collins FM, Rima BK. 2002. Modulating the function of the measles virus RNA-dependent RNA polymerase by insertion of green flu-orescent protein into the open reading frame. J Virol 76:7322-7328. http://dx.doi.org/10.1128/JVI.76.14.7322-7328.2002.
41. Ruedas JB, Perrault J. 2009. Insertion of enhanced green fluorescent protein in a hinge region of vesicular stomatitis virus L polymerase protein creates a temperature-sensitive virus that displays no virion-associated polymerase activity in vitro. J Virol 83:12241-12252. http://dx.doi.org/10.1128/JVI.01273-09.
42. Finke S, Brzozka K, Conzelmann KK. 2004. Tracking fluorescencelabeled rabies virus: enhanced green fluorescent protein-tagged phosphoprotein P supports virus gene expression and formation of infectious particles. J Virol 78:12333-12343. http://dx.doi.org/10.1128/JVI.78.22.12333-12343.2004.
43. Lahaye X, Vidy A, Fouquet B, Blondel D. 2012. Hsp70 protein positively regulates rabies virus infection. J Virol 86:4743-4751. http://dx.doi.org/10.1128/JVI.06501-11.
44. Zhang X, Bourhis JM, Longhi S, Carsillo T, Buccellato M, Morin B, Canard B, Oglesbee M. 2005. Hsp72 recognizes a P binding motif in the measles virus N protein C-terminus. Virology 337:162-174. http://dx.doi.org/10.1016/j.virol.2005.03.035.
45. Zhang X, Glendening C, Linke H, Parks CL, Brooks C, Udem SA, 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. http://dx.doi.org/10.1128/JVI.76.17.8737-8746.2002.
46. Smith DR, McCarthy S, Chrovian A, Olinger G, Stossel A, Geisbert TW, Hensley LE, Connor JH. 2010. Inhibition of heat-shock protein 90 reduces Ebola virus replication. Antiviral Res 87:187-194. http://dx.doi.org/10.1016/j.antiviral.2010.04.015.
47. Chase G, Deng T, Fodor E, Leung BW, Mayer D, Schwemmle M, Brownlee G. 2008. Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 377:431-439. http://dx.doi.org/10.1016/j.virol.2008.04.040.
48. Momose F, Naito T, Yano K, Sugimoto S, Morikawa Y, Nagata K. 2002. Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis. J Biol Chem 277:45306-45314. http://dx.doi.org/10.1074/jbc.M206822200.
49. Manzoor R, Kuroda K, Yoshida R, Tsuda Y, Fujikura D, Miyamoto H, Kajihara M, Kida H, Takada A. 2014. Heat shock protein 70 modulates influenza A virus polymerase activity. J Biol Chem 289:7599-7614. http://dx.doi.org/10.1074/jbc.M113.507798.