Rhinovirus 3C Protease Facilitates Specific Nucleoporin Cleavage and Mislocalisation of Nuclear Proteins in Infected Host Cells

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Walker, Erin J ^a   Younessi, Parisa ^a   Fulcher, Alex J ^b   McCuaig, Robert ^a   Thomas, Belinda J ^c   Bardin, Philip G ^c   Jans, David A ^b   Ghildyal, Reena ^a  

^a UNIVERSITY OF CANBERRA   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c MONASH MEDICAL CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

3C PROTEASE; NUCLEAR PROTEIN; NUCLEOLIN; NUCLEOPORIN; NUCLEOPORIN 153; NUCLEOPORIN 62; NUCLEOPORIN 98; PROTEINASE; SC35 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; RHINOVIRUS INFECTION; VIRUS PATHOGENESIS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BLOTTING, WESTERN; CELL NUCLEOLUS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; COS CELLS; CYSTEINE ENDOPEPTIDASES; CYTOPLASM; GREEN FLUORESCENT PROTEINS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR SPACE; MICROSCOPY, CONFOCAL; NUCLEAR PORE COMPLEX PROTEINS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROTEOLYSIS; RHINOVIRUS; RIBONUCLEOPROTEINS; RNA-BINDING PROTEINS; TRANSFECTION; VIRAL PROTEINS;

EID: 84881340606     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071316     Document Type: Article

References (43)

1. Johnston SL, Pattemore PK, Sanderson G, Smith S, Lampe F, et al. (1995) Community study of role of viral infections in exacerbations of asthma in 9-11 year old children. BMJ 310: 1225-1229.
2. Kaur B, Anderson HR, Austin J, Burr M, Harkins LS, et al. (1998) Prevalence of asthma symptoms, diagnosis, and treatment in 12-14 year old children across Great Britain (international study of asthma and allergies in childhood, ISAAC UK). BMJ 316: 118-124.
3. Racaniello VR (2001) Picornaviridae: the viruses and their replication. In: Knipe DM, Howley PM, editors. Fields Virology, 4th Edition. Philadelphia, PA: Lippincott/Raven. 685-722.
4. Brunel F, Zakin MM, Buc H, Buckle M, (1996) The Polypyrimidine Tract Binding (PTB) Protein Interacts With Single-Stranded DNA in a Sequence-Specific Manner. Nucleic Acids Research 24: 1608-1615.
5. Nagy PD, Wang RY, Pogany J, Hafren A, Makinen K, (2011) Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology 411: 374-382.
6. Niepmann M, (2010) Internal translation initiation of picornaviruses and hepatitis C virus. Biochimica et Biophysica Acta (BBA)- Gene Regulatory Mechanisms 1789: 529-541.
7. Alvisi G, Rawlinson SM, Ghildyal R, Ripalti A, Jans DA, (2008) Regulated nucleocytoplasmic trafficking of viral gene products: a therapeutic target? Biochim Biophys Acta 1784: 213-227.
8. Fulcher AJ, Jans DA, (2011) Regulation of nucleocytoplasmic trafficking of viral proteins: an integral role in pathogenesis? Biochim Biophys Acta 1813: 2176-2190.
9. Ghildyal R, Ho A, Dias M, Soegiyono L, Bardin PG, et al. (2009) The respiratory syncytial virus matrix protein possesses a Crm1-mediated nuclear export mechanism. J Virol 83: 5353-5362.
10. Ghildyal R, Jordan B, Li D, Dagher H, Bardin PG, et al. (2009) Rhinovirus 3C protease can localize in the nucleus and alter active and passive nucleocytoplasmic transport. J Virol 83: 7349-7352.
11. Hearps AC, Jans DA, (2006) HIV-1 integrase is capable of targeting DNA to the nucleus via an importin alpha/beta-dependent mechanism. Biochem J 398: 475-484.
12. Pryor MJ, Rawlinson SM, Butcher RE, Barton CL, Waterhouse TA, et al. (2007) Nuclear localization of dengue virus nonstructural protein 5 through its importin alpha/beta-recognized nuclear localization sequences is integral to viral infection. Traffic 8: 795-807.
13. Oksayan S, Ito N, Moseley G, Blondel D, (2011) Subcellular trafficking in rhabdovirus infection and immune evasion: a novel target for therapeutics. Infect Disord Drug Targets 12: 38-58.
14. See H, Wark P, (2008) Innate immune response to viral infection of the lungs. Paediatr Respir Rev 9: 243-250.
15. Hetzer MW, Wente SR, (2009) Border control at the nucleus: biogenesis and organization of the nuclear membrane and pore complexes. Dev Cell 17: 606-616.
16. Donnelly M, Gani D, Flint M, Monaghan S, Ryan M, (1997) The cleavage activities of aphthovirus and cardiovirus 2A proteins. J Gen Virol 78: 13-21.
17. Gustin KE, Sarnow P, (2001) Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. Embo J 20: 240-249.
18. Lidsky PV, Hato S, Bardina MV, Aminev AG, Palmenberg AC, et al. (2006) Nucleocytoplasmic traffic disorder induced by cardioviruses. J Virol 80: 2705-2717.
19. Amineva SP, Aminev AG, Palmenberg AC, Gern JE, (2004) Rhinovirus 3C protease precursors 3CD and 3CD' localize to the nuclei of infected cells. J Gen Virol 85: 2969-2979.
20. Gustin KE, (2003) Inhibition of nucleo-cytoplasmic trafficking by RNA viruses: targeting the nuclear pore complex. Virus Research 95: 35-44.
21. Gustin KE, Sarnow P, (2002) Inhibition of nuclear import and alteration of nuclear pore complex composition by rhinovirus. J Virol 76: 8787-8796.
22. Park N, Skern T, Gustin KE, (2010) Specific Cleavage of the Nuclear Pore Complex Protein Nup62 by a Viral Protease. Journal of Biological Chemistry 285: 28796-28805.
23. Mosser AG, Brockman-Schneider R, Amineva S, Burchell L, Sedgwick JB, et al. (2002) Similar frequency of rhinovirus-infectible cells in upper and lower airway epithelium. J Infect Dis 185: 734-743.
24. Ghildyal R, Ho A, Wagstaff KM, Dias MM, Barton CL, et al. (2005) Nuclear import of the respiratory syncytial virus matrix protein is mediated by importin beta1 independent of importin alpha. Biochemistry 44: 12887-12895.
25. Mahy BW, Kangro HO (1996) Virology Methods Manual. New York, NY: Harcourt Brace. 25-46 p.
26. Lee WM, Monroe SS, Rueckert RR, (1993) Role of maturation cleavage in infectivity of picornaviruses: activation of an infectosome. J Virol 67: 2110-2122.
27. Ghildyal R, Dagher H, Donninger H, de Silva D, Li X, et al. (2005) Rhinovirus infects primary human airway fibroblasts and induces a neutrophil chemokine and a permeability factor. J Med Virol 75: 608-615.
28. Hames BD, Rickwood D. (1998) Gel Electrophoresis of Proteins: A Practical Approach: Oxford University Press.
29. Park N, Katikaneni P, Skern T, Gustin KE, (2008) Differential targeting of nuclear pore complex proteins in poliovirus-infected cells. J Virol 82: 1647-1655.
30. Chatel G, Desai SH, Mattheyses AL, Powers MA, Fahrenkrog B, (2011) Domain topology of nucleoporin Nup98 within the nuclear pore complex. J Struct Biol 177: 81-89.
31. Park N, Skern T, Gustin KE, (2010) Specific cleavage of the nuclear pore complex protein Nup62 by a viral protease. J Biol Chem 285: 28796-28805.
32. Xu S, Powers MA, (2009) Nuclear pore proteins and cancer. Semin Cell Dev Biol 20: 620-630.
33. Belov GA, Lidsky PV, Mikitas OV, Egger D, Lukyanov KA, et al. (2004) Bidirectional Increase in Permeability of Nuclear Envelope upon Poliovirus Infection and Accompanying Alterations of Nuclear Pores. J Virol 78: 10166-10177.
34. Lin S, Coutinho-Mansfield G, Wang D, Pandit S, Fu XD, (2008) The splicing factor SC35 has an active role in transcriptional elongation. Nat Struct Mol Biol 15: 819-826.
35. Fu XD, (1993) Specific commitment of different pre-mRNAs to splicing by single SR proteins. Nature 365: 82-85.
36. Dreyfuss G, Kim VN, Kataoka N, (2002) Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3: 195-205.
37. Cammas A, Pileur F, Bonnal S, Lewis SM, Leveque N, et al. (2007) Cytoplasmic Relocalization of Heterogeneous Nuclear Ribonucleoprotein A1 Controls Translation Initiation of Specific mRNAs. Mol Biol Cell 18: 5048-5059.
38. Fridell RA, Truant R, Thorne L, Benson RE, Cullen BR, (1997) Nuclear import of hnRNP A1 is mediated by a novel cellular cofactor related to karyopherin-beta. J Cell Sci 110 (Pt 11): 1325-1331.
39. Truant R, Fridell RA, Benson RE, Bogerd H, Cullen BR, (1998) Identification and functional characterization of a novel nuclear localization signal present in the yeast Nab2 poly(A)+ RNA binding protein. Mol Cell Biol 18: 1449-1458.
40. Waggoner S, Sarnow P, (1998) Viral ribonucleoprotein complex formation and nucleolar-cytoplasmic relocalization of nucleolin in poliovirus-infected cells. J Virol 72: 6699-6709.
41. Cancio-Lonches C, Yocupicio-Monroy M, Sandoval-Jaime C, Galvan-Mendoza I, Urena L, et al. (2011) Nucleolin interacts with the feline calicivirus 3′ untranslated region and the protease-polymerase NS6 and NS7 proteins, playing a role in virus replication. J Virol 85: 8056-8068.
42. Binford SL, Maldonado F, Brothers MA, Weady PT, Zalman LS, et al. (2005) Conservation of amino acids in human rhinovirus 3C protease correlates with broad-spectrum antiviral activity of rupintrivir, a novel human rhinovirus 3C protease inhibitor. Antimicrob Agents Chemother 49: 619-626.
43. Watters K, Palmenberg AC, (2011) Differential processing of nuclear pore complex proteins by rhinovirus 2A proteases from different species and serotypes. J Virol 85: 10874-10883.