1887

Abstract

Early during infection, the herpes simplex regulatory protein ICP0 promotes the proteasome-dependent degradation of a number of cellular proteins and the loss of a number of SUMO-1-modified protein isoforms, including PML. Recently, ICP0 has been shown to induce the accumulation of conjugated ubiquitin and function as a ubiquitin E3 ligase. However, certain aspects of the biochemistry, cell biology and the links between SUMO-1 conjugation/deconjugation and protein degradation remain unclear. For example, it is not currently known whether SUMO-1 deconjugation is a prerequisite for ubiquitination or degradation and, if so, by what mechanism this may occur. To help address these questions, a SUMO-specific protease (SENP1) was cloned and its expression and localization in relation to ICP0 examined. A cell line was established which constitutively expresses SUMO-1 to facilitate studies of localization and biochemistry. SENP1 localized to the nucleus mainly in discrete subdomains, a subset of which co-localized with the PML bodies. Both ICP0 and SENP1 protease promoted the loss of SUMO-1 from the nucleus, observed both for the endogenous species and the cell line expressing the epitope-tagged SUMO-1. The tagged SUMO-1 was recruited into high molecular mass conjugates in the cell line, and expression of SENP1 promoted loss of these species, including the modified species of PML. Finally, in co-transfection experiments ICP0 promoted the recruitment of SENP1 to nuclear domains, a result which was also observed early during infection. The significance of these findings is discussed in relation to the function of ICP0.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-12-2951
2002-12-01
2020-07-11
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/12/0832951a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-12-2951&mimeType=html&fmt=ahah

References

  1. Aravind L., Koonin E. V.. 2000; The U box is a modified RING finger – a common domain in ubiquitination. Current Biology10:R132–134
    [Google Scholar]
  2. Batchelor A. H., O’Hare P.. 1992; Localization of cis -acting sequence requirements in the promoter of the latency-associated transcript of herpes simplex virus type 1 required for cell-type-specific activity. Journal of Virology66:3573–3582
    [Google Scholar]
  3. Boddy M. N., Howe K., Etkin L. D., Solomon E., Freemont P. S.. 1996; PIC 1, a novel ubiquitin-like protein which interacts with the PML component of a multiprotein complex that is disrupted in acute promyelocytic leukaemia. Oncogene13:971–982
    [Google Scholar]
  4. Boutell C., Sadis S., Everett R. D.. 2002; Herpes simplex virus type 1 immediate-early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases in vitro . Journal of Virology76:841–850
    [Google Scholar]
  5. Cai W., Astor L. A., Liptak L. M., Cho C., Coen D. M., Schaffer P. A.. 1993; The herpes simplex virus type 1 regulatory protein ICP0 enhances virus replication during acute infection and reactivation from latency. Journal of Virology67:7501–7512
    [Google Scholar]
  6. Clements G. B., Stow N. D.. 1989; A herpes simplex virus type 1 mutant containing a deletion within immediate early gene 1 is latency-competent in mice. Journal of General Virology70:2501–2506
    [Google Scholar]
  7. Desterro J. M., Rodriguez M. S., Hay R. T.. 1998; SUMO-1 modification of IκBα inhibits NF-κB activation. Molecular Cell2:233–239
    [Google Scholar]
  8. Everett R. D.. 2000; ICP0 induces the accumulation of co-localizing conjugated ubiquitin. Journal of Virology74:9994–10005
    [Google Scholar]
  9. Everett R. D., Maul G. G.. 1994; HSV-1 IE protein Vmw110 causes redistribution of PML. EMBO Journal13:5062–5069
    [Google Scholar]
  10. Everett R., O’Hare P., O’Rourke D., Barlow P., Orr A.. 1995; Point mutations in the herpes simplex virus type 1 Vmw110 RING finger helix affect activation of gene expression, viral growth, and interaction with PML-containing nuclear structures. Journal of Virology69:7339–7344
    [Google Scholar]
  11. Everett R. D., Meredith M., Orr A., Cross A., Kathoria M., Parkinson J.. 1997; A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein. EMBO Journal16:1519–1530
    [Google Scholar]
  12. Everett R. D., Freemont P., Saitoh H., Dasso M., Orr A., Kathoria M., Parkinson J.. 1998; The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110- and proteasome-dependent loss of several PML isoforms. Journal of Virology72:6581–6591
    [Google Scholar]
  13. Everett R. D., Earnshaw W. C., Findlay J., Lomonte P.. 1999a; Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO Journal18:1526–1538
    [Google Scholar]
  14. Everett R. D., Meredith M., Orr A.. 1999b; The ability of herpes simplex virus type 1 immediate-early protein Vmw110 to bind to a ubiquitin-specific protease contributes to its roles in the activation of gene expression and stimulation of virus replication. Journal of Virology73:417–426
    [Google Scholar]
  15. Freemont P. S.. 2000; RING for destruction?. Current Biology10:R84–87
    [Google Scholar]
  16. Gong L., Millas S., Maul G. G., Yeh E. T.. 2000; Differential regulation of sentrinized proteins by a novel sentrin-specific protease. Journal of Biological Chemistry275:3355–3359
    [Google Scholar]
  17. Hang J., Dasso M.. 2002; Association of the human SUMO-1 protease SENP2 with the nuclear pore. Journal of Biological Chemistry277:19961–19966
    [Google Scholar]
  18. Harris R. A., Everett R. D., Zhu X. X., Silverstein S., Preston C. M.. 1989; Herpes simplex virus type 1 immediate-early protein Vmw110 reactivates latent herpes simplex virus type 2 in an in vitro latency system. Journal of Virology63:3513–3515
    [Google Scholar]
  19. Ishov A. M., Maul G. G.. 1996; The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. Journal of Cell Biology134:815–826
    [Google Scholar]
  20. Ishov A. M., Sotnikov A. G., Negorev D., Vladimirova O. V., Neff N., Kamitani T., Yeh E. T., Strauss J. F.III., Maul G. G.. 1999; PML is critical for ND10 formation and recruits the PML-interacting protein Daxx to this nuclear structure when modified by SUMO-1. Journal of Cell Biology147:221–234
    [Google Scholar]
  21. Kamitani T., Kito K., Nguyen H. P., Wada H., Fukuda-Kamitani T., Yeh E. T.. 1998a; Identification of three major sentrinization sites in PML. Journal of Biological Chemistry273:26675–26682
    [Google Scholar]
  22. Kamitani T., Nguyen H. P., Kito K., Fukuda-Kamitani T., Yeh E. T.. 1998b; Covalent modification of PML by the sentrin family of ubiquitin-like proteins. Journal of Biological Chemistry273:3117–3120
    [Google Scholar]
  23. Kawaguchi Y., Bruni R., Roizman B.. 1997; Interaction of herpes simplex virus 1 α regulatory protein ICP0 with elongation factor 1 Δ: ICP0 affects translational machinery. Journal of Virology71:1019–1024
    [Google Scholar]
  24. Kim K. I., Baek S. H., Jeon Y. J., Nishimori S., Suzuki T., Uchida S., Shimbara N., Saitoh H., Tanaka K., Chung C. H.. 2000; A new SUMO-1-specific protease, SUSP1, that is highly expressed in reproductive organs. Journal of Biological Chemistry275:14102–14106
    [Google Scholar]
  25. Lallemand-Breitenbach V., Zhu J., Puvion F., Koken M., Honore N., Doubeikovsky A., Duprez E., Pandolfi P. P., Puvion E., Freemont P., de The H.. 2001; Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As2O3-induced PML or PML/retinoic acid receptor α degradation. Journal of Experimental Medicine193:1361–1371
    [Google Scholar]
  26. Leib D. A., Coen D. M., Bogard C. L., Hicks K. A., Yager D. R., Knipe D. M., Tyler K. L., Schaffer P. A.. 1989; Immediate-early regulatory gene mutants define different stages in the establishment and reactivation of herpes simplex virus latency. Journal of Virology63:759–768
    [Google Scholar]
  27. Leppard K. N., Everett R. D.. 1999; The adenovirus type 5 E1b 55K and E4 Orf3 proteins associate in infected cells and affect ND10 components. Journal of General Virology80:997–1008
    [Google Scholar]
  28. Li S. J., Hochstrasser M.. 1999; A new protease required for cell-cycle progression in yeast. Nature398:246–251
    [Google Scholar]
  29. Li S. J., Hochstrasser M.. 2000; The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Molecular and Cellular Biology20:2367–2377
    [Google Scholar]
  30. Lomonte P., Sullivan K. F., Everett R. D.. 2001; Degradation of nucleosome-associated centromeric histone H3-like protein CENP-A induced by herpes simplex virus type 1 protein ICP0. Journal of Biological Chemistry276:5829–5835
    [Google Scholar]
  31. Mahajan R., Delphin C., Guan T., Gerace L., Melchior F.. 1997; A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell88:97–107
    [Google Scholar]
  32. Matunis M. J., Coutavas E., Blobel G.. 1996; A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. Journal of Cell Biology135:1457–1470
    [Google Scholar]
  33. Maul G. G.. 1998; Nuclear domain 10, the site of DNA virus transcription and replication. Bioessays20:660–667
    [Google Scholar]
  34. Müller S., Matunis M. J., Dejean A.. 1998; Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO Journal17:61–70
    [Google Scholar]
  35. Okura T., Gong L., Kamitani T., Wada T., Okura I., Wei C. F., Chang H. M., Yeh E. T.. 1996; Protection against Fas/APO-1- and tumour necrosis factor-mediated cell death by a novel protein, sentrin. Journal of Immunology157:4277–4281
    [Google Scholar]
  36. O’Rourke D., O’Hare P.. 1993; Mutually exclusive binding of two cellular factors within a critical promoter region of the gene for the IE110k protein of herpes simplex virus. Journal of Virology67:7201–7214
    [Google Scholar]
  37. O’Rourke D., Elliott G., Papworth M., Everett R., O’Hare P.. 1998; Examination of determinants for intranuclear localization and transactivation within the RING finger of herpes simplex virus type 1 IE110k protein. Journal of General Virology79:537–548
    [Google Scholar]
  38. Parkinson J., Everett R. D.. 2000; Alphaherpesvirus proteins related to herpes simplex virus type 1 ICP0 affect cellular structures and proteins. Journal of Virology74:10006–10017
    [Google Scholar]
  39. Parkinson J., Lees-Miller S. P., Everett R. D.. 1999; Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA- dependent protein kinase. Journal of Virology73:650–657
    [Google Scholar]
  40. Roizman B., Sears A. E.. 1996; The replication of herpes simplex viruses. In Fields Virology pp2231–2295 Edited by Fields B. N., Knipe D. M., Howley P.. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  41. Sacks W. R., Schaffer P. A.. 1987; Deletion mutants in the gene encoding the herpes simplex virus type 1 immediate-early protein ICP0 exhibit impaired growth in cell culture. Journal of Virology61:829–839
    [Google Scholar]
  42. Saitoh H., Hinchey J.. 2000; Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. Journal of Biological Chemistry275:6252–6258
    [Google Scholar]
  43. Stow N. D., Stow E. C.. 1986; Isolation and characterization of a herpes simplex virus type 1 mutant containing a deletion within the gene encoding the immediate early polypeptide Vmw110. Journal of General Virology67:2571–2585
    [Google Scholar]
  44. Suzuki T., Ichiyama A., Saitoh H., Kawakami T., Omata M., Chung C. H., Kimura M., Shimbara N., Tanaka K.. 1999; A new 30-kDa ubiquitin-related SUMO-1 hydrolase from bovine brain. Journal of Biological Chemistry274:31131–31134
    [Google Scholar]
  45. Tyers M., Jorgensen P.. 2000; Proteolysis and the cell cycle: with this RING I do thee destroy. Current Opinion in Genetics & Development10:54–64
    [Google Scholar]
  46. Van Sant C., Hagglund R., Lopez P., Roizman B.. 2001; The infected cell protein 0 of herpes simplex virus 1 dynamically interacts with proteasomes, binds and activates the cdc34 E2 ubiquitin-conjugating enzyme, and possesses in vitro E3 ubiquitin ligase activity. Proceedings of the National Academy of Sciences, USA98:8815–8820
    [Google Scholar]
  47. Zhong S., Muller S., Ronchetti S., Freemont P. S., Dejean A., Pandolfi P. P.. 2000; Role of SUMO-1-modified PML in nuclear body formation. Blood95:2748–2752
    [Google Scholar]
  48. Zhu X. X., Chen J. X., Young C. S., Silverstein S.. 1990; Reactivation of latent herpes simplex virus by adenovirus recombinants encoding mutant IE-0 gene products. Journal of Virology64:4489–4498
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-12-2951
Loading
/content/journal/jgv/10.1099/0022-1317-83-12-2951
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error