Fusion of a fluorescent protein to the pUL25 minor capsid protein of pseudorabies virus allows live-cell capsid imaging with negligible impact on infection

References

1. Antinone S. E., Smith G. A. 2010; Retrograde axon transport of herpes simplex virus and pseudorabies virus: a live-cell comparative analysis. J Virol 84:1504–1512 [View Article][PubMed]
   [Google Scholar]
2. Antinone S. E., Shubeita G. T., Coller K. E., Lee J. I., Haverlock-Moyns S., Gross S. P., Smith G. A. 2006; The herpesvirus capsid surface protein, VP26, and the majority of the tegument proteins are dispensable for capsid transport toward the nucleus. J Virol 80:5494–5498 [View Article][PubMed]
   [Google Scholar]
3. Cockrell S. K., Sanchez M. E., Erazo A., Homa F. L. 2009; Role of the UL25 protein in herpes simplex virus DNA encapsidation. J Virol 83:47–57 [View Article][PubMed]
   [Google Scholar]
4. Coller K. E., Lee J. I., Ueda A., Smith G. A. 2007; The capsid and tegument of the alphaherpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J Virol 81:11790–11797 [View Article][PubMed]
   [Google Scholar]
5. Conway J. F., Cockrell S. K., Copeland A. M., Newcomb W. W., Brown J. C., Homa F. L. 2010; Labeling and localization of the herpes simplex virus capsid protein UL25 and its interaction with the two triplexes closest to the penton. J Mol Biol 397:575–586 [View Article][PubMed]
   [Google Scholar]
6. Demmin G. L., Clase A. C., Randall J. A., Enquist L. W., Banfield B. W. 2001; Insertions in the gG gene of pseudorabies virus reduce expression of the upstream Us3 protein and inhibit cell-to-cell spread of virus infection. J Virol 75:10856–10869 [View Article][PubMed]
   [Google Scholar]
7. Desai P. J. 2000; A null mutation in the UL36 gene of herpes simplex virus type 1 results in accumulation of unenveloped DNA-filled capsids in the cytoplasm of infected cells. J Virol 74:11608–11618 [View Article][PubMed]
   [Google Scholar]
8. Desai P., Person S. 1998; Incorporation of the green fluorescent protein into the herpes simplex virus type 1 capsid. J Virol 72:7563–7568[PubMed]
   [Google Scholar]
9. Forest T., Barnard S., Baines J. D. 2005; Active intranuclear movement of herpesvirus capsids. Nat Cell Biol 7:429–431 [View Article][PubMed]
   [Google Scholar]
10. Fossum E., Friedel C. C., Rajagopala S. V., Titz B., Baiker A., Schmidt T., Kraus T., Stellberger T., Rutenberg C.other authors 2009; Evolutionarily conserved herpesviral protein interaction networks. PLoS Pathog 5:e1000570 [View Article][PubMed]
    [Google Scholar]
11. Frampton A. R. Jr, Uchida H., von Einem J., Goins W. F., Grandi P., Cohen J. B., Osterrieder N., Glorioso J. C. 2010; Equine herpesvirus type 1 (EHV-1) utilizes microtubules, dynein, and ROCK1 to productively infect cells. In Vet Microbiol 14112–21 [View Article]
    [Google Scholar]
12. Fuchs W., Klupp B. G., Granzow H., Mettenleiter T. C. 2004; Essential function of the pseudorabies virus UL36 gene product is independent of its interaction with the UL37 protein. J Virol 78:11879–11889 [View Article][PubMed]
    [Google Scholar]
13. Gibson W., Roizman B. 1972; Proteins specified by herpes simplex virus. 8. Characterization and composition of multiple capsid forms of subtypes 1 and 2. J Virol 10:1044–1052[PubMed]
    [Google Scholar]
14. Granzow H., Klupp B. G., Mettenleiter T. C. 2005; Entry of pseudorabies virus: an immunogold-labeling study. J Virol 79:3200–3205 [View Article][PubMed]
    [Google Scholar]
15. Heine J. W., Honess R. W., Cassai E., Roizman B. 1974; Proteins specified by herpes simplex virus. XII. The virion polypeptides of type 1 strains. J Virol 14:640–651[PubMed]
    [Google Scholar]
16. Knipe D. M., Batterson W., Nosal C., Roizman B., Buchan A. 1981; Molecular genetics of herpes simplex virus. VI. Characterization of a temperature-sensitive mutant defective in the expression of all early viral gene products. J Virol 38:539–547[PubMed]
    [Google Scholar]
17. Krautwald M., Maresch C., Klupp B. G., Fuchs W., Mettenleiter T. C. 2008; Deletion or green fluorescent protein tagging of the pUL35 capsid component of pseudorabies virus impairs virus replication in cell culture and neuroinvasion in mice. J Gen Virol 89:1346–1351 [View Article][PubMed]
    [Google Scholar]
18. Luxton G. W., Haverlock S., Coller K. E., Antinone S. E., Pincetic A., Smith G. A. 2005; Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc Natl Acad Sci U S A 102:5832–5837 [View Article][PubMed]
    [Google Scholar]
19. McNab A. R., Desai P., Person S., Roof L. L., Thomsen D. R., Newcomb W. W., Brown J. C., Homa F. L. 1998; The product of the herpes simplex virus type 1 UL25 gene is required for encapsidation but not for cleavage of replicated viral DNA. J Virol 72:1060–1070[PubMed]
    [Google Scholar]
20. McNabb D. S., Courtney R. J. 1992; Characterization of the large tegument protein (ICP1/2) of herpes simplex virus type 1. Virology 190:221–232 [View Article][PubMed]
    [Google Scholar]
21. Newcomb W. W., Brown J. C. 2010; Structure and capsid association of the herpesvirus large tegument protein UL36. J Virol 84:9408–9414 [View Article][PubMed]
    [Google Scholar]
22. Newcomb W. W., Homa F. L., Brown J. C. 2006; Herpes simplex virus capsid structure: DNA packaging protein UL25 is located on the external surface of the capsid near the vertices. J Virol 80:6286–6294 [View Article][PubMed]
    [Google Scholar]
23. O’Hara M., Rixon F. J., Stow N. D., Murray J., Murphy M., Preston V. G. 2010; Mutational analysis of the herpes simplex virus type 1 UL25 DNA packaging protein reveals regions that are important after the viral DNA has been packaged. J Virol 84:4252–4263 [View Article][PubMed]
    [Google Scholar]
24. Pasdeloup D., Blondel D., Isidro A. L., Rixon F. J. 2009; Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J Virol 83:6610–6623 [View Article][PubMed]
    [Google Scholar]
25. Shaner N. C., Campbell R. E., Steinbach P. A., Giepmans B. N. G., Palmer A. E., Tsien R. Y. 2004; Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22:1567–1572 [View Article][PubMed]
    [Google Scholar]
26. Sheaffer A. K., Newcomb W. W., Gao M., Yu D., Weller S. K., Brown J. C., Tenney D. J. 2001; Herpes simplex virus DNA cleavage and packaging proteins associate with the procapsid prior to its maturation. J Virol 75:687–698 [View Article][PubMed]
    [Google Scholar]
27. Smith G. A., Banfield B. W. 2006; The development and use of alpha-herpesviruses-expressing fluorescent proteins. In Alpha Herpesviruses: Molecular and Cell Biology pp. 205–217 Edited by Sandri-Golden R. M. UK: Caister Academic Press;
    [Google Scholar]
28. Smith G. A., Enquist L. W. 1999; Construction and transposon mutagenesis in Escherichia coli of a full-length infectious clone of pseudorabies virus, an alphaherpesvirus. J Virol 73:6405–6414[PubMed]
    [Google Scholar]
29. Smith G. A., Enquist L. W. 2000; A self-recombining bacterial artificial chromosome and its application for analysis of herpesvirus pathogenesis. Proc Natl Acad Sci U S A 97:4873–4878 [View Article][PubMed]
    [Google Scholar]
30. Smith B. N., Banfield B. W., Smeraski C. A., Wilcox C. L., Dudek F. E., Enquist L. W., Pickard G. E. 2000; Pseudorabies virus expressing enhanced green fluorescent protein: a tool for in vitro electrophysiological analysis of transsynaptically labeled neurons in identified central nervous system circuits. Proc Natl Acad Sci U S A 97:9264–9269 [View Article][PubMed]
    [Google Scholar]
31. Smith G. A., Gross S. P., Enquist L. W. 2001; Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc Natl Acad Sci U S A 98:3466–3470 [View Article][PubMed]
    [Google Scholar]
32. Smith G. A., Pomeranz L., Gross S. P., Enquist L. W. 2004; Local modulation of plus-end transport targets herpesvirus entry and egress in sensory axons. Proc Natl Acad Sci U S A 101:16034–16039 [View Article][PubMed]
    [Google Scholar]
33. Thurlow J. K., Rixon F. J., Murphy M., Targett-Adams P., Hughes M., Preston V. G. 2005; The herpes simplex virus type 1 DNA packaging protein UL17 is a virion protein that is present in both the capsid and the tegument compartments. J Virol 79:150–158 [View Article][PubMed]
    [Google Scholar]
34. Toropova K., Huffman J. B., Homa F. L., Conway J. F. 2011; The herpes simplex virus 1 UL17 protein is the second constituent of the capsid vertex-specific component required for DNA packaging and retention. J Virol 85:7513–7522 [View Article][PubMed]
    [Google Scholar]
35. Trus B. L., Newcomb W. W., Cheng N., Cardone G., Marekov L., Homa F. L., Brown J. C., Steven A. C. 2007; Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-filled HSV-1 capsids. Mol Cell 26:479–489 [View Article][PubMed]
    [Google Scholar]
36. Uetz P., Dong Y. A., Zeretzke C., Atzler C., Baiker A., Berger B., Rajagopala S. V., Roupelieva M., Rose D.other authors 2006; Herpesviral protein networks and their interaction with the human proteome. Science 311:239–242 [View Article][PubMed]
    [Google Scholar]
37. Ward P. L., Ogle W. O., Roizman B. 1996; Assemblons: nuclear structures defined by aggregation of immature capsids and some tegument proteins of herpes simplex virus 1. J Virol 70:4623–4631[PubMed]
    [Google Scholar]
38. Wingfield P. T., Stahl S. J., Thomsen D. R., Homa F. L., Booy F. P., Trus B. L., Steven A. C. 1997; Hexon-only binding of VP26 reflects differences between the hexon and penton conformations of VP5, the major capsid protein of herpes simplex virus. J Virol 71:8955–8961[PubMed]
    [Google Scholar]
39. Wolfstein A., Nagel C. H., Radtke K., Döhner K., Allan V. J., Sodeik B. 2006; The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 7:227–237 [View Article][PubMed]
    [Google Scholar]
40. Zhou Z. H., He J., Jakana J., Tatman J. D., Rixon F. J., Chiu W. 1995; Assembly of VP26 in herpes simplex virus-1 inferred from structures of wild-type and recombinant capsids. Nat Struct Biol 2:1026–1030 [View Article][PubMed]
    [Google Scholar]