Identifying the ERAD ubiquitin E3 ligases for viral and cellular targeting of MHC class I

Molecular Immunology

Volumn 68, Issue 2, 2015, Pages 106-111

  Van den Boomen, D J H ^a   Lehner, P J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

E3 ubiquitin ligase; ER associated degradation; HRD1; Human cytomegalovirus; TMEM129; TRC8; Viral immune evasion

Indexed keywords

BLOOD CLOTTING FACTOR; INTEGRIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NECTIN 2; THROMBOMODULIN; TRC8 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ALPHA INTEGRIN; CELL SURFACE RECEPTOR; HLA ANTIGEN CLASS 1; IL2RB PROTEIN, HUMAN; INTERLEUKIN 2 RECEPTOR BETA; RNA BINDING PROTEIN; RNF139 PROTEIN, HUMAN; THBD PROTEIN, HUMAN; TMEM129 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE; US11 PROTEIN, HERPESVIRUS; US2 PROTEIN, VARICELLOVIRUS; VIRAL PROTEIN; VIRUS ENVELOPE PROTEIN;

ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; AUTOREGULATION; COMPLEX FORMATION; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN TARGETING; UBIQUITINATION; US11 GENE; US2 GENE; VIRUS GENE; CYTOMEGALOVIRUS; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION;

CYTOMEGALOVIRUS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HOST-PATHOGEN INTERACTIONS; HUMANS; INTEGRIN ALPHA CHAINS; INTERLEUKIN-2 RECEPTOR BETA SUBUNIT; PROTEOLYSIS; RECEPTORS, CELL SURFACE; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; THROMBOMODULIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS;

EID: 84957435967     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2015.07.005     Document Type: Article

References (34)

1. Ben-Arieh, S.V., Zimerman, B., Smorodinsky, N.I., Yaacubovicz, M., Schechter, C., Bacik, I., Gibbs, J., Bennink, J.R., Yewdell, J.W., Coligan, J.E., Firat, H., Lemonnier, F., Ehrlich, R., 2001. Human cytomegalovirus protein US2 interferes with the expression of human HFE, a nonclassical class I major histocompatibility complex molecule that regulates iron homeostasis. J. Virol. 75, 10557-10562.
2. Bernasconi, R., Galli, C., Kokame, K., Molinari, M., 2013. Autoadaptive ER-associated degradation defines a preemptive unfolded protein response pathway. Mol. Cell 52, 783-793.
3. Boname, J.M., Bloor, S., Wandel, M.P., Nathan, J.A., Antrobus, R., Dingwell, K.S., Thurston, T.L., Smith, D.L., Smith, J.C., Randow, F., Lehner, P.J., 2014. Cleavage by signal peptide peptidase is required for the degradation of selected tail-anchored proteins. J. Cell Biol. 205, 847-862.
4. Burr, M.L., Cano, F., Svobodova, S., Boyle, L.H., Boname, J.M., Lehner, P.J., 2011. HRD1 and UBE2J1 target misfolded MHC class I heavy chains for endoplasmic reticulum-associated degradation. Proc. Natl. Acad. Sci. 108, 2034-2039, U S A.
5. Burr, M.L., van den Boomen, D.J., Bye, H., Antrobus, R., Wiertz, E.J., Lehner, P.J., 2013. MHC class I molecules are preferentially ubiquitinated on endoplasmic reticulum luminal residues during HRD1 ubiquitin E3 ligase-mediated dislocation. Proc. Natl. Acad. Sci. 110, 14290-14295, U S A.
6. Cadwell, K., Coscoy, L., 2005. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science, 127-130.
7. Cali, T., Galli, C., Olivari, S., Molinari, M., 2008. Segregation and rapid turnover of EDEM1 by an autophagy-like mechanism modulates standard ERAD and folding activities. Biochem. Biophys. Res. Commun. 371, 405-410.
8. Chen, C.Y., Malchus, N.S., Hehn, B., Stelzer, W., Avci, D., Langosch, D., Lemberg, M.K., 2014. Signal peptide peptidase functions in ERAD to cleave the unfolded protein response regulator XBP1u. EMBO J. 33, 2492-2506.
9. Fleig, L., Bergbold, N., Sahasrabudhe, P., Geiger, B., Kaltak, L., Lemberg, M.K., 2012. Ubiquitin-dependent intramembrane rhomboid protease promotes ERAD of membrane proteins. Mol. Cell 47, 558-569.
10. Furman, M.H., Loureiro, J., Ploegh, H.L., Tortorella, D., 2003. Ubiquitinylation of the cytosolic domain of a type I membrane protein is not required to initiate its dislocation from the endoplasmic reticulum. J. Biol. Chem. 278, 34804-34811.
11. Hansen, T.H., Bouvier, M., 2009. MHC class I antigen presentation: learning from viral evasion strategies. Nat. Rev. Immunol. 9, 503-513.
12. Hassink, G.C., Barel, M.T., Van Voorden, S.B., Kikkert, M., Wiertz, E.J., 2006. Ubiquitination of MHC class I heavy chains is essential for dislocation by human cytomegalovirus-encoded US2 but not US11. J. Biol. Chem. 281, 30063-30071.
13. Hegde, R.S., Ploegh, H.L., 2010. Quality and quantity control at the endoplasmic reticulum. Curr. Opin. Cell Biol. 22, 437-446.
14. Hsu, J.L., van den Boomen, D.J., Tomasec, P., Weekes, M.P., Antrobus, R., Stanton, R.J., Ruckova, E., Sugrue, D., Wilkie, G.S., Davison, A.J., Wilkinson, G.W., Lehner, P.J., 2015. Plasma membrane profiling defines an expanded class of cell surface proteins selectively targeted for degradation by HCMV US2 in cooperation with UL141. PLoS Pathog. 11, e1004811.
15. Irisawa, M., Inoue, J., Ozawa, N., Mori, K., Sato, R., 2009. The sterol-sensing endoplasmic reticulum (ER) membrane protein TRC8 hampers ER to golgi transport of sterol regulatory element-binding protein-2 (SREBP-2)/SREBP cleavage-activated protein and reduces SREBP-2 cleavage. J. Biol. Chem. 284, 28995-29004.
16. Jo, Y., Lee, P.C., Sguigna, P.V., DeBose-Boyd, R.A., 2011. Sterol-induced degradation of HMG CoA reductase depends on interplay of two Insigs and two ubiquitin ligases, gp78 and Trc8. Proc. Natl. Acad. Sci. U S A 108, 20503-20508.
17. Kikkert, M., Hassink, G., Barel, M., Hirsch, C., van der Wal, F.J., Wiertz, E., 2001. Ubiquitination is essential for human cytomegalovirus US11-mediated dislocation of MHC class I molecules from the endoplasmic reticulum to the cytosol. Biochem. J. 358, 369-377.
18. Lee, J.P., Brauweiler, A., Rudolph, M., Hooper, J.E., Drabkin, H.A., Gemmill, R.M., 2010. The TRC ubiquitin ligase is sterol regulated and interacts with lipid and protein biosynthetic pathways. Mol. Cancer Res. 8, 93-106, 8.
19. Lilley, B.N., Ploegh, H.L., 2004. A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429, 834-840.
20. Lilley, B.N., Tortorella, D., Ploegh, H.L., 2003. Dislocation of a type I membrane protein requires interactions between membrane-spanning segments within the lipid bilayer. Mol. Biol. Cell 14, 3690-3698.
21. Loureiro, J., Lilley, B.N., Spooner, E., Noriega, V., Tortorella, D., Ploegh, H.L., 2006. Signal peptide peptidase is required for dislocation from the endoplasmic reticulum. Nature 441, 894-897.
22. Loureiro, J., Ploegh, H.L., 2006. Antigen presentation and the ubiquitin-proteasome system in host-pathogen interactions. Adv. Immunol. 92, 225-305.
23. Mueller, B., Lilley, B.N., Ploegh, H.L., 2006. SEL1L, the homologue of yeast Hrd3p, is involved in protein dislocation from the mammalian ER. J. Cell Biol. 175, 261-270.
24. Olzmann, J.A., Kopito, R.R., Christianson, J.C., 2013. The mammalian endoplasmic reticulum-associated degradation system. Cold Spring Harb. Perspect. Biol. 5.
25. Prod'homme, V., Sugrue, D.M., Stanton, R.J., Nomoto, A., Davies, J., Rickards, C.R., Cochrane, D., Moore, M., Wilkinson, G.W., Tomasec, P., 2010. Human cytomegalovirus UL141 promotes efficient downregulation of the natural killer cell activating ligand CD112. J. Gen. Virol., 2034-2039.
26. Randow, F., Lehner, P.J., 2009. Viral avoidance and exploitation of the ubiquitin system. Nat. Cell Biol. 11, 527-534.
27. Stagg, H.R., Thomas, M., van den Boomen, D., Wiertz, E.J., Drabkin, H.A., Gemmill, R.M., Lehner, P.J., 2009. The TRC8 E3 ligase ubiquitinates MHC class I molecules before dislocation from the ER. J. Cell Biol. 186, 685-692.
28. Tomazin, R., Boname, J., Hegde, N.R., Lewinsohn, D.M., Altschuler, Y., Jones, T.R., Cresswell, P., Nelson, J.A., Riddell, S.R., Johnson, D.C., 1999. Cytomegalovirus US2 destroys two components of the MHC class II pathway, preventing recognition by CD4+ T cells. Nat. Med. 5, 1039-1043.
29. Tsai, Y.C., Leichner, G.S., Pearce, M.M., Wilson, G.L., Wojcikiewicz, R.J., Roitelman, J., Weissman, A.M., 2012. Differential regulation of HMG-CoA reductase and Insig-1 by enzymes of the ubiquitin-proteasome system. Mol. Biol. Cell 23, 4484-4494.
30. van de Weijer, M.L., Bassik, M.C., Luteijn, R.D., Voorburg, C.M., Lohuis, M.A., Kremmer, E., Hoeben, R.C., LeProust, E.M., Chen, S., Hoelen, H., Ressing, M.E., Patena, W., Weissman, J.S., McManus, M.T., Wiertz, E.J., Lebbink, R.J., 2014. A high-coverage shRNA screen identifies TMEM129 as an E3 ligase involved in ER-associated protein degradation. Nat. Commun. 5, 3832.
31. van den Boomen, D.J., Timms, R.T., Grice, G.L., Stagg, H.R., Skodt, K., Dougan, G., Nathan, J.A., Lehner, P.J., 2014. TMEM129 is a Derlin-1 associated ERAD E3 ligase essential for virus-induced degradation of MHC-I. Proc. Natl. Acad. Sci. U S A 111, 11425-11430.
32. Wang, X., Herr, R.A., Rabelink, M., Hoeben, R.C., Wiertz, E.J., Hansen, T.H., 2009. Ube2j2 ubiquitinates hydroxylated amino acids on ER-associated degradation substrates. J. Cell Biol. 187, 655-668.
33. Wiertz, E.J., Jones, T.R., Sun, L., Bogyo, M., Geuze, H.J., Ploegh, H.L., 1996a. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84, 769-779.
34. Wiertz, E.J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T.R., Rapoport, T.A., Ploegh, H.L., 1996b. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384, 432-438.