1887

Abstract

The receptor internalization and degradation (RID) complex of adenovirus plays an important role in modulating the immune response by downregulating the surface levels of tumour necrosis factor receptor 1 (TNFR1), thereby inhibiting NF-B activation. Total cellular content of TNFR1 is also reduced in the presence of RID, which can be inhibited by treatment with lysosomotropic agents. In this report, surface biotinylation experiments revealed that, although RID and TNFR1 were able to form a complex on the cell surface, the rate of TNFR1 endocytosis was not affected by RID. However, the degradation of internalized TNFR1 was enhanced significantly in the presence of RID. Therefore, these data suggest that RID downregulates TNFR1 levels by altering the fate of internalized TNFR1 that becomes associated with RID at the plasma membrane, probably by promoting its sorting into endosomal/lysosomal degradation compartments.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82001-0
2006-11-01
2019-11-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/11/3161.html?itemId=/content/journal/jgv/10.1099/vir.0.82001-0&mimeType=html&fmt=ahah

References

  1. Benedict, C. A., Norris, P. S., Prigozy, T. I. & 7 other authors ( 2001; ). Three adenovirus E3 proteins cooperate to evade apoptosis by tumor necrosis factor-related apoptosis-inducing ligand receptor-1 and -2. J Biol Chem 276, 3270–3278.[CrossRef]
    [Google Scholar]
  2. Carlin, C. R., Tollefson, A. E., Brady, H. A., Hoffman, B. L. & Wold, W. S. M. ( 1989; ). Epidermal growth factor receptor is down-regulated by a 10,400 MW protein encoded by the E3 region of adenovirus. Cell 57, 135–144.[CrossRef]
    [Google Scholar]
  3. Chin, Y. R. & Horwitz, M. S. ( 2005; ). Mechanism for removal of tumor necrosis factor receptor 1 from the cell surface by the adenovirus RIDα/β complex. J Virol 79, 13606–13617.[CrossRef]
    [Google Scholar]
  4. Crooks, D., Kil, S. J., McCaffery, J. M. & Carlin, C. ( 2000; ). E3-13.7 integral membrane proteins encoded by human adenoviruses alter epidermal growth factor receptor trafficking by interacting directly with receptors in early endosomes. Mol Biol Cell 11, 3559–3572.[CrossRef]
    [Google Scholar]
  5. Delgado-Lopez, F. & Horwitz, M. S. ( 2006; ). Adenovirus RIDαβ complex inhibits lipopolysaccharide signaling without altering TLR4 cell surface expression. J Virol 80, 6378–6386.[CrossRef]
    [Google Scholar]
  6. Efrat, S., Fejer, G., Brownlee, M. & Horwitz, M. S. ( 1995; ). Prolonged survival of pancreatic islet allografts mediated by adenovirus immunoregulatory transgenes. Proc Natl Acad Sci U S A 92, 6947–6951.[CrossRef]
    [Google Scholar]
  7. Efrat, S., Serreze, D., Svetlanov, A., Post, C. M., Johnson, E. A., Herold, K. & Horwitz, M. S. ( 2001; ). Adenovirus early region 3 (E3) immunomodulatory genes decrease the incidence of autoimmune diabetes in NOD mice. Diabetes 50, 980–984.[CrossRef]
    [Google Scholar]
  8. Elsing, A. & Burgert, H.-G. ( 1998; ). The adenovirus E3/10.4K–14.5K proteins down-modulate the apoptosis receptor Fas/Apo-1 by inducing its internalization. Proc Natl Acad Sci U S A 95, 10072–10077.[CrossRef]
    [Google Scholar]
  9. Fessler, S. P., Chin, Y. R. & Horwitz, M. S. ( 2004a; ). Inhibition of tumor necrosis factor (TNF) signal transduction by the adenovirus group C RID complex involves downregulation of surface levels of TNF receptor 1. J Virol 78, 13113–13121.[CrossRef]
    [Google Scholar]
  10. Fessler, S. P., Delgado-Lopez, F. & Horwitz, M. S. ( 2004b; ). Mechanisms of E3 modulation of immune and inflammatory responses. Curr Top Microbiol Immunol 273, 113–135.
    [Google Scholar]
  11. Herbein, G. & O'Brien, W. A. ( 2000; ). Tumor necrosis factor (TNF)-α and TNF receptors in viral pathogenesis. Proc Soc Exp Biol Med 223, 241–257.[CrossRef]
    [Google Scholar]
  12. Higuchi, M. & Aggarwal, B. B. ( 1994; ). TNF induces internalization of the p60 receptor and shedding of the p80 receptor. J Immunol 152, 3550–3558.
    [Google Scholar]
  13. Hilgendorf, A., Lindberg, J., Ruzsics, Z., Höning, S., Elsing, A., Löfqvist, M., Engelmann, H. & Burgert, H.-G. ( 2003; ). Two distinct transport motifs in the adenovirus E3/10.4-14.5 proteins act in concert to down-modulate apoptosis receptors and the epidermal growth factor receptor. J Biol Chem 278, 51872–51884.[CrossRef]
    [Google Scholar]
  14. Hoffman, P. & Carlin, C. ( 1994; ). Adenovirus E3 protein causes constitutively internalized epidermal growth factor receptors to accumulate in a prelysosomal compartment, resulting in enhanced degradation. Mol Cell Biol 14, 3695–3706.
    [Google Scholar]
  15. Hoffman, B. L., Ullrich, A., Wold, W. S. M. & Carlin, C. R. ( 1990; ). Retrovirus-mediated transfer of an adenovirus gene encoding an integral membrane protein is sufficient to down regulate the receptor for epidermal growth factor. Mol Cell Biol 10, 5521–5524.
    [Google Scholar]
  16. Horwitz, M. S. ( 2004; ). Function of adenovirus E3 proteins and their interactions with immunoregulatory cell proteins. J Gene Med 6, S172–S183.[CrossRef]
    [Google Scholar]
  17. Krajcsi, P. & Wold, W. S. M. ( 1992; ). The adenovirus E3-14.5K protein which is required for prevention of TNF cytolysis and for down-regulation of the EGF receptor contains phosphoserine. Virology 187, 492–498.[CrossRef]
    [Google Scholar]
  18. Krajcsi, P., Tollefson, A. E. & Wold, W. S. M. ( 1992; ). The E3–14.5K integral membrane protein of adenovirus that is required for down-regulation of the EGF receptor and for prevention of TNF cytolysis is O-glycosylated but not N-glycosylated. Virology 188, 570–579.[CrossRef]
    [Google Scholar]
  19. Lichtenstein, D. L., Doronin, K., Toth, K., Kuppuswamy, M., Wold, W. S. M. & Tollefson, A. E. ( 2004; ). Adenovirus E3-6.7K protein is required in conjunction with the E3-RID protein complex for the internalization and degradation of TRAIL receptor 2. J Virol 78, 12297–12307.[CrossRef]
    [Google Scholar]
  20. Mayor, S., Presley, J. F. & Maxfield, F. R. ( 1993; ). Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. J Cell Biol 121, 1257–1269.[CrossRef]
    [Google Scholar]
  21. Pierce, M. A., Chapman, H. D., Post, C. M., Svetlanov, A., Efrat, S., Horwitz, M. & Serreze, D. V. ( 2003; ). Adenovirus early region 3 antiapoptotic 10.4K, 14.5K, and 14.7K genes decrease the incidence of autoimmune diabetes in NOD mice. Diabetes 52, 1119–1127.[CrossRef]
    [Google Scholar]
  22. Porteu, F. & Hieblot, C. ( 1994; ). Tumor necrosis factor induces a selective shedding of its p75 receptor from human neutrophils. J Biol Chem 269, 2834–2840.
    [Google Scholar]
  23. Shisler, J., Yang, C., Walter, B., Ware, C. F. & Gooding, L. R. ( 1997; ). The adenovirus E3-10.4K/14.5K complex mediates loss of cell surface Fas (CD95) and resistance to Fas-induced apoptosis. J Virol 71, 8299–8306.
    [Google Scholar]
  24. Tollefson, A. E., Krajcsi, P., Pursley, M. H., Gooding, L. R. & Wold, W. S. M. ( 1990; ). A 14,500 MW protein is coded by region E3 of group C human adenoviruses. Virology 175, 19–29.[CrossRef]
    [Google Scholar]
  25. Tollefson, A. E., Stewart, A. R., Yei, S., Saha, S. K. & Wold, W. S. M. ( 1991; ). The 10,400- and 14,500-dalton proteins encoded by region E3 of adenovirus form a complex and function together to down-regulate the epidermal growth factor receptor. J Virol 65, 3095–3105.
    [Google Scholar]
  26. Tollefson, A. E., Hermiston, T. W., Lichtenstein, D. L. & 7 other authors ( 1998; ). Forced degradation of Fas inhibits apoptosis in adenovirus-infected cells. Nature 392, 726–730.[CrossRef]
    [Google Scholar]
  27. Tollefson, A. E., Toth, K., Doronin, K., Kuppuswamy, M., Doronina, O. A., Lichtenstein, D. L., Hermiston, T. W., Smith, C. A. & Wold, W. S. M. ( 2001; ). Inhibition of TRAIL-induced apoptosis and forced internalization of TRAIL receptor 1 by adenovirus proteins. J Virol 75, 8875–8887.[CrossRef]
    [Google Scholar]
  28. von Herrath, M. G., Efrat, S., Oldstone, M. B. A. & Horwitz, M. S. ( 1997; ). Expression of adenoviral E3 transgenes in β cells prevents autoimmune diabetes. Proc Natl Acad Sci U S A 94, 9808–9813.[CrossRef]
    [Google Scholar]
  29. Yoshie, O., Tada, K. & Ishida, N. ( 1986; ). Binding and crosslinking of 125I-labeled recombinant human tumor necrosis factor to cell surface receptors. J Biochem (Tokyo) 100, 531–541.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.82001-0
Loading
/content/journal/jgv/10.1099/vir.0.82001-0
Loading

Data & Media loading...

Most Cited This Month

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