Resolution of the cellular proteome of the nucleocapsid protein from a highly pathogenic isolate of porcine reproductive and respiratory syndrome virus identifies PARP-1 as a cellular target whose interaction is critical for virus biology

Veterinary Microbiology

Volumn 176, Issue 1-2, 2015, Pages 109-119

  Liu, Long ^a   Lear, Zoe ^b   Hughes, David J ^b   Wu, Weining ^c   Zhou, En min ^a   Whitehouse, Adrian ^b   Chen, Hongying ^a   Hiscox, Julian A ^a,c,d  

^a NORTHWEST A F UNIVERSITY   (China)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

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

Author keywords

3 AB; Antivirus; Nucleocapsid; PARP 1; Proteome; PRRSV

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NUCLEOCAPSID PROTEIN; PROTEOME; VIRUS RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BINDING;

ARTERIVIRUS; ARTICLE; CONTROLLED STUDY; HOST CELL; HUMAN; HUMAN CELL; NONHUMAN; PHENOTYPE; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; VIROGENESIS; VIRUS GENOME; VIRUS ISOLATION; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOGENICITY; PIG; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; VIRULENCE;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE;

ANIMALS; GENE EXPRESSION REGULATION; NUCLEOCAPSID PROTEINS; POLY(ADP-RIBOSE) POLYMERASES; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; PROTEIN BINDING; PROTEOME; PROTEOMICS; SWINE; VIRULENCE;

EID: 84922936239     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2014.11.023     Document Type: Article

References (36)

1. Baillie J.K., Digard P. Influenza - time to target the host?. N. Engl. J. Med. 2013, 369:191-193.
2. Bortz E., Westera L., Maamary J., Steel J., Albrecht R.A., Manicassamy B., Chase G., Martinez-Sobrido L., Schwemmle M., Garcia-Sastre A. Host- and strain-specific regulation of influenza virus polymerase activity by interacting cellular proteins. mBio 2011, 2. e00151-11.
3. Bueno M.T., Reyes D., Valdes L., Saheba A., Urias E., Mendoza C., Fregoso O.I., Llano M. Poly(ADP-ribose) polymerase 1 promotes transcriptional repression of integrated retroviruses. J. Virol. 2013, 87:2496-2507.
4. Chase G., Deng T., Fodor E., Leung B.W., Mayer D., Schwemmle M., Brownlee G. Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 2008, 377:431-439.
5. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26:1367-1372.
6. Dove B.K., Surtees R., Bean T.J., Munday D., Wise H.M., Digard P., Carroll M.W., Ajuh P., Barr J.N., Hiscox J.A. A quantitative proteomic analysis of lung epithelial (A549) cells infected with 2009 pandemic influenza A virus using stable isotope labelling with amino acids in cell culture. Proteomics 2012, 12:1431-1436.
7. Emmott E., Rodgers M.A., Macdonald A., McCrory S., Ajuh P., Hiscox J.A. Quantitative proteomics using stable isotope labeling with amino acids in cell culture reveals changes in the cytoplasmic, nuclear, and nucleolar proteomes in Vero cells infected with the coronavirus infectious bronchitis virus. Mol. Cell. Proteomics 2010, 9:1920-1936.
8. Emmott E., Munday D., Bickerton E., Britton P., Rodgers M.A., Whitehouse A., Zhou E.M., Hiscox J.A. The cellular interactome of the coronavirus infectious bronchitis virus nucleocapsid protein and functional implications for virus biology. J. Virol. 2013, 87:9486-9500.
9. Garcia-Dorival I., Wu W., Dowall S., Armstrong S., Touzelet O., Wastling J., Barr J.N., Matthews D., Carroll M., Newson R., Hiscox J.A. Elucidation of the Ebola virus VP24 cellular interactome and disruption of virus biology through targeted inhibition of host-cell protein function. J. Proteome Res. 2014, 13:5120-5135.
10. Geller R., Andino R., Frydman J. Hsp90 inhibitors exhibit resistance-free antiviral activity against respiratory syncytial virus. PLOS ONE 2013, 8:e56762.
11. Grady S.L., Hwang J., Vastag L., Rabinowitz J.D., Shenk T. Herpes simplex virus 1 infection activates poly(ADP-ribose) polymerase and triggers the degradation of poly(ADP-ribose) glycohydrolase. J. Virol. 2012, 86:8259-8268.
12. Jourdan S.S., Osorio F., Hiscox J.A. 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 2012, 12:1015-1023.
13. Jourdan S.S., Osorio F.A., Hiscox J.A. Biophysical characterisation of the nucleocapsid protein from a highly pathogenic porcine reproductive and respiratory syndrome virus strain. Biochem. Biophys. Res. Commun. 2012, 419:137-141.
14. Lahaye X., Vidy A., Fouquet B., Blondel D. Hsp70 protein positively regulates rabies virus infection. J. Virol. 2012, 86:4743-4751.
15. Lee S.M., Kleiboeker S.B. Porcine reproductive and respiratory syndrome virus induces apoptosis through a mitochondria-mediated pathway. Virology 2007, 365:419-434.
16. Lee C., Hodgins D., Calvert J.G., Welch S.K., Jolie R., Yoo D. Mutations within the nuclear localization signal of the porcine reproductive and respiratory syndrome virus nucleocapsid protein attenuate virus replication. Virology 2006, 346:238-250.
17. Li Y.H., Tas A., Snijder E.J., Fang Y. Identification of porcine reproductive and respiratory syndrome virus ORF1a-encoded non-structural proteins in virus-infected cells. J. Gen. Virol. 2012, 93:829-839.
18. Liu Y., Shi W., Zhou E., Wang S., Hu S., Cai X., Rong F., Wu J., Xu M., Xu M., Li L. Dynamic changes in inflammatory cytokines in pigs infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Clin. Vaccin. Immunol. 2010, 17:1439-1445.
19. Munday D.C., Emmott E., Surtees R., Lardeau C.H., Wu W., Duprex W.P., Dove B.K., Barr J.N., Hiscox J.A. Quantitative proteomic analysis of A549 cells infected with human respiratory syncytial virus. Mol. Cell. Proteomics 2010, 9:2438-2459.
20. Munday D.C., Wu W., Smith N., Fix J., Noton S.L., Galloux M., Touzelet O., Armstrong S.D., Dawson J.M., Aljabr W., Easton A.J., Rameix-Welti M.A., de Oliveira A.P., Simabuco F., Ventura A.M., Hughes D.J., Barr J.N., Fearns R., Digard P., Eléouët J.F., Hiscox J.A. Interactome analysis of the human respiratory syncytial virus RNA polymerase complex identifies protein chaperones as important co-factors that promote L protein stability and RNA synthesis. J. Virol. 2014, 89:917-930.
21. Music N., Gagnon C.A. The role of porcine reproductive and respiratory syndrome (PRRS) virus structural and non-structural proteins in virus pathogenesis. Anim. Health Res. Rev. 2010, 11:135-163.
22. Ohsaki E., Ueda K., Sakakibara S., Do E., Yada K., Yamanishi K. Poly(ADP-ribose) polymerase 1 binds to Kaposi's sarcoma-associated herpesvirus (KSHV) terminal repeat sequence and modulates KSHV replication in latency. J. Virol. 2004, 78:9936-9946.
23. Pei Y., Hodgins D.C., Lee C., Calvert J.G., Welch S.K., Jolie R., Keith M., Yoo D. Functional mapping of the porcine reproductive and respiratory syndrome virus capsid protein nuclear localization signal and its pathogenic association. Virus Res. 2008, 135:107-114.
24. Purnell M.R., Whish W.J. Novel inhibitors of poly(ADP-ribose) synthetase. Biochem. J. 1980, 185:775-777.
25. Radhakrishnan A., Yeo D., Brown G., Myaing M.Z., Iyer L.R., Fleck R., Tan B.H., Aitken J., Sanmun D., Tang K., Yarwood A., Brink J., Sugrue R.J. Protein analysis of purified respiratory syncytial virus particles reveals an important role for heat shock protein 90 in virus particle assembly. Mol. Cell. Proteomics 2010, 9:1829-1848.
26. Rowland R.R., Kervin R., Kuckleburg C., Sperlich A., Benfield D.A. The localization of porcine reproductive and respiratory syndrome virus nucleocapsid protein to the nucleolus of infected cells and identification of a potential nucleolar localization signal sequence. Virus Res. 1999, 64:1-12.
27. Smith D.R., McCarthy S., Chrovian A., Olinger G., Stossel A., Geisbert T.W., Hensley L.E., Connor J.H. Inhibition of heat-shock protein 90 reduces Ebola virus replication. Antiviral Res. 2010, 87:187-194.
28. Song C., Lu R., Bienzle D., Liu H.C., Yoo D. Interaction of the porcine reproductive and respiratory syndrome virus nucleocapsid protein with the inhibitor of MyoD family-a domain-containing protein. Biol. Chem. 2009, 390:215-223.
29. Song B.H., Kim J.M., Kim J.K., Jang H.S., Yun G.N., Choi E.J., Song J.Y., Yun S.I., Lee Y.M. Packaging of porcine reproductive and respiratory syndrome virus replicon RNA by a stable cell line expressing its nucleocapsid protein. J. Microbiol. 2011, 49:516-523.
30. Sun Y., Han M., Kim C., Calvert J.G., Yoo D. Interplay between interferon-mediated innate immunity and porcine reproductive and respiratory syndrome virus. Viruses 2012, 4:424-446.
31. Tempera I., Deng Z., Atanasiu C., Chen C.J., D'Erme M., Lieberman P.M. Regulation of Epstein-Barr virus OriP replication by poly(ADP-ribose) polymerase 1. J. Virol. 2010, 84:4988-4997.
32. Trinkle-Mulcahy L., Boulon S., Lam Y.W., Urcia R., Boisvert F.M., Vandermoere F., Morrice N.A., Swift S., Rothbauer U., Leonhardt H., Lamond A. Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. J. Cell Biol. 2008, 183:223-239.
33. Wang X., Bai J., Zhang L., Wang X., Li Y., Jiang P. Poly(A)-binding protein interacts with the nucleocapsid protein of porcine reproductive and respiratory syndrome virus and participates in viral replication. Antiviral Res. 2012, 96:315-323.
34. Wu W., Tran K.C., Teng M.N., Heesom K.J., Matthews D.A., Barr J.N., Hiscox J.A. The interactome of the human respiratory syncytial virus NS1 protein highlights multiple effects on host cell biology. J. Virol. 2012, 86:7777-7789.
35. Xiao S., Zhang A., Zhang C., Ni H., Gao J., Wang C., Zhao Q., Wang X., Wang X., Ma C., Liu H., Li N., Mu Y., Sun Y., Zhang G., Hiscox J.A., Hsu W.H., Zhou E.M. Heme oxygenase-1 acts as an antiviral factor for porcine reproductive and respiratory syndrome virus infection and over-expression inhibits virus replication in vitro. Antiviral Res. 2014, 110:60-69.
36. Yoo D., Wootton S.K., Li G., Song C., Rowland R.R. Colocalization and interaction of the porcine arterivirus nucleocapsid protein with the small nucleolar RNA-associated protein fibrillarin. J. Virol. 2003, 77:12173-12183.