Variation in the nuclear effects of infection by different human rhinovirus serotypes

Frontiers in Microbiology

Volumn 6, Issue AUG, 2015, Pages

  Walker, Erin J ^a   Jensen, Lora M ^a   Croft, Sarah ^a   Ghildyal, Reena ^a  

^a UNIVERSITY OF CANBERRA   (Australia)

Author keywords

Human rhinovirus; Nuclear transport; Nucleoporin; Serotype; Viral proteases

Indexed keywords

NUCLEOLIN;

ARTICLE; CONTROLLED STUDY; DISEASE COURSE; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REAL TIME POLYMERASE CHAIN REACTION; RHINOVIRUS INFECTION; RNA ISOLATION; RNA REPLICATION; SEQUENCE ANALYSIS; SEROTYPE; VIRUS LOAD; WESTERN BLOTTING;

EID: 84940930324     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00875     Document Type: Article

References (34)

1. Amineva, S.P., Aminev, A.G., Palmenberg, A.C., and Gern, J.E. (2004). Rhinovirus 3C protease precursors 3CD and 3CD' localize to the nuclei of infected cells. J. Gen. Virol. 85(Pt 10), 2969-2979. doi: 10.1099/vir.0.80164-0.
2. Andries, K., Dewindt, B., Snoeks, J., Wouters, L., Moereels, H., Lewi, P.J., et al. (1990). Two groups of rhinoviruses revealed by a panel of antiviral compounds present sequence divergence and differential pathogenicity. J. Virol. 64, 1117-1123.
3. Bushell, M., Wood, W., Carpenter, G., Pain, V.M., Morley, S.J., and Clemens, M.J. (2001). Disruption of the interaction of mammalian protein synthesis eukaryotic initiation factor 4B with the poly(A)-binding protein by caspase- and viral protease-mediated cleavages. J. Biol. Chem. 276, 23922-23928. doi: 10.1074/jbc.M100384200.
4. Dagher, H., Donninger, H., Hutchinson, P., Ghildyal, R., and Bardin, P. (2004). Rhinovirus detection: comparison of real-time and conventional PCR. J. Virol. Methods 117, 113-121. doi: 10.1016/j.jviromet.2004.01.003.
5. Denlinger, L.C., Sorkness, R.L., Lee, W.M., Evans, M.D., Wolff, M.J., Mathur, S.K., et al. (2011). Lower airway rhinovirus burden and the seasonal risk of asthma exacerbation. Am. J. Respir. Crit. Care Med. 184, 1007-1014. doi: 10.1164/rccm.201103-0585OC.
6. Ghildyal, R., Dagher, H., Donninger, H., de Silva, D., Li, X., Freezer, N.J., et al. (2005). Rhinovirus infects primary human airway fibroblasts and induces a neutrophil chemokine and a permeability factor. J. Med. Virol. 75, 608-615. doi: 10.1002/jmv.20315.
7. Greco, A., Arata, L., Soler, E., Gaume, X., Coute, Y., Hacot, S., et al. (2012). Nucleolin interacts with US11 protein of herpes simplex virus 1 and is involved in its trafficking. J. Virol. 86, 1449-1457. doi: 10.1128/JVI. 06194-11.
8. Gustin, K.E., and Sarnow, P. (2001). Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. EMBO J. 20, 240-249. doi: 10.1093/emboj/20.1.240.
9. Gustin, K.E., and Sarnow, P. (2002). Inhibition of nuclear import and alteration of nuclear pore complex composition by rhinovirus. J. Virol. 76, 8787-8796. doi: 10.1128/JVI.76.17.8787-8796.2002.
10. Hames, B.D. (1998). Gel Electrophoresis of Proteins: A Practical Approach. Oxford, NY: Oxford University Press.
11. Iwane, M.K., Prill, M.M., Lu, X., Miller, E.K., Edwards, K.M., Hall, C.B., et al. (2011). Human rhinovirus species associated with hospitalizations for acute respiratory illness in young US children. J. Infect. Dis. 204, 1702-1710. doi: 10.1093/infdis/jir634.
12. Kito, S., Shimizu, K., Okamura, H., Yoshida, K., Morimoto, H., Fujita, M., et al. (2003). Cleavage of nucleolin and argyrophilic nucleolar organizer region associated proteins in apoptosis-induced cells. Biochem. Biophys. Res. Commun. 300, 950-956. doi: 10.1016/S0006-291X(02)02942-X.
13. Kuyumcu-Martinez, N.M., Van, M.E., Eden, Younan, P., and Lloyd, R.E. (2004). Cleavage of poly(A)-binding protein by poliovirus 3C protease inhibits host cell translation: a novel mechanism for host translation shutoff. Mol. Cell. Biol. 24, 1779-1790. doi: 10.1128/MCB.24.4.1779-1790.2004.
14. Lamphear, B.J., Yan, R., Yang, F., Waters, D., Liebig, H.D., Klump, H., et al. (1993). Mapping the cleavage site in protein synthesis initiation factor eIF-4 gamma of the 2A proteases from human Coxsackievirus and rhinovirus. J. Biol. Chem. 268, 19200-19203.
15. Lee, W.M., Lemanske, R.F. Jr., Evans, M.D., Vang, F., Pappas, T., Gangnon, R., et al. (2012). Human rhinovirus species and season of infection determine illness severity. Am. J. Respir. Crit. Care Med. 186, 886-891. doi: 10.1164/rccm.201202-0330OC.
16. Liebig, H.D., Ziegler, E., Yan, R., Hartmuth, K., Klump, H., Kowalski, H., et al. (1993). Purification of two picornaviral 2A proteinases: interaction with eIF-4 gamma and influence on in vitro translation. Biochemistry 32, 7581-7588. doi: 10.1021/bi00080a033.
17. Mahy, B.W., and Kangro, H.O. (1996). Virology Methods Manual. New York, NY, Harcourt Brace.
18. Maldarelli, F., Xiang, C., Chamoun, G., and Zeichner, S.L. (1998). The expression of the essential nuclear splicing factor SC35 is altered by human immunodeficiency virus infection. Virus Res. 53, 39-51. doi: 10.1016/S0168-1702(97)00130-5.
19. McBride, A.E., Schlegel, A., and Kirkegaard, K. (1996). Human protein Sam68 relocalization and interaction with poliovirus RNA polymerase in infected cells. Proc. Natl. Acad. Sci. U.S.A. 93, 2296-2301. doi: 10.1073/pnas.93.6.2296.
20. McFarlane, M., and Graham, S.V. (2010). Human papillomavirus regulation of SR proteins. Biochem. Soc. Trans. 38, 1116-1121. doi: 10.1042/BST0381116.
21. Meerovitch, K., Svitkin, Y.V., Lee, H.S., Lejbkowicz, F., Kenan, D.J., Chan, E.K., et al. (1993). La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J. Virol. 67, 3798-3807.
22. Nakagome, K., Bochkov, Y.A., Ashraf, S., Brockman-Schneider, R.A., Evans, M.D., Pasic, T.R., et al. (2014). Effects of rhinovirus species on viral replication and cytokine production. J. Allergy Clin. Immunol. 134, 332-341. doi: 10.1016/j.jaci.2014.01.029.
23. Nakielny, S., and Dreyfuss, G. (1996). The hnRNP C proteins contain a nuclear retention sequence that can override nuclear export signals. J. Cell Biol. 134, 1365-1373. doi: 10.1083/jcb.134.6.1365.
24. Oksayan, S., Nikolic, J., David, C.T., Blondel, D., Jans, D.A., and Moseley, G.W. (2015). Identification of a role for nucleolin in rabies virus infection. J. Virol. 89, 1939-1943. doi: 10.1128/JVI. 03320-14.
25. Palmenberg, A.C., Spiro, D., Kuzmickas, R., Wang, S., Djikeng, A., Rathe, J.A., et al. (2009). Sequencing and analyses of all known human rhinovirus genomes reveal structure and evolution. Science 324, 55-59. doi: 10.1126/science.1165557.
26. Rajan, D., McCracken, C.E., Kopleman, H.B., Kyu, S.Y., Lee, F.E., Lu, X., et al. (2014). Human rhinovirus induced cytokine/chemokine responses in human airway epithelial and immune cells. PLoS ONE 9:e114322. doi: 10.1371/journal.pone.0114322.
27. Schuler, B.A., Schreiber, M.T., Li, L., Mokry, M., Kingdon, M.L., Raugi, D.N., et al. (2014). Major and minor group rhinoviruses elicit differential signaling and cytokine responses as a function of receptor-mediated signal transduction. PLoS ONE 9:e93897. doi: 10.1371/journal.pone.0093897.
28. Strang, B.L., Boulant, S., Kirchhausen, T., and Coen, D.M. (2012). Host cell nucleolin is required to maintain the architecture of human cytomegalovirus replication compartments. mBio 3:e00301-11. doi: 10.1128/mBio.00301-11.
29. Su, P.Y., Wang, Y.F., Huang, S.W., Lo, Y.C., Wang, Y.H., Wu, S.R., et al. (2015). Cell surface nucleolin facilitates enterovirus 71 binding and infection. J. Virol. 89, 4527-4538. doi: 10.1128/JVI. 03498-14.
30. Tayyari, F., Marchant, D., Moraes, T.J., Duan, W., Mastrangelo, P., and Hegele, R.G. (2011). Identification of nucleolin as a cellular receptor for human respiratory syncytial virus. Nat. Med. 17, 1132-1135. doi: 10.1038/nm.2444.
31. Vlasak, M., Roivainen, M., Reithmayer, M., Goesler, I., Laine, P., Snyers, L., et al. (2005). The minor receptor group of human rhinovirus (HRV) includes HRV23 and HRV25, but the presence of a lysine in the VP1 HI loop is not sufficient for receptor binding. J. Virol. 79, 7389-7395. doi: 10.1128/JVI.79.12.7389-7395.2005.
32. Walker, E.J., Younessi, P., Fulcher, A.J., McCuaig, R., Thomas, B.J., Bardin, P.G., et al. (2013). Rhinovirus 3C protease facilitates specific nucleoporin cleavage and mislocalisation of nuclear proteins in infected host cells. PLoS ONE 8:e71316. doi: 10.1371/journal.pone.0071316.
33. Wark, P.A., Grissell, T., Davies, B., See, H., and Gibson, P.G. (2009). Diversity in the bronchial epithelial cell response to infection with different rhinovirus strains. Respirology 14, 180-186. doi: 10.1111/j.1440-1843.2009.01480.x.
34. Watters, K., and Palmenberg, A.C. (2011). Differential processing of nuclear pore complex proteins by rhinovirus 2A proteases from different species and serotypes. J. Virol. 85, 10874-10883. doi: 10.1128/JVI. 00718-11.