Stabilization of an E3 ligase-E2-ubiquitin complex increases cell surface MHC class I expression

Journal of Immunology

Volumn 184, Issue 12, 2010, Pages 6978-6985

  Duncan, Lidia M ^a   Nathan, James A ^a   Lehner, Paul J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ISOLEUCINE; K3 UBIQUITIN E3 LIGASE; MUTANT PROTEIN; UBIQUITIN CONJUGATING ENZYME 13; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CAPSULAR POLYSACCHARIDE K3; CD99 PROTEIN, HUMAN; CELL ADHESION MOLECULE; HLA ANTIGEN CLASS 1; LEUKOCYTE ANTIGEN; UBIQUITIN; VIRUS ANTIGEN;

ALLELE; AMINO ACID SUBSTITUTION; ARTICLE; BIODEGRADATION; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; ENZYME SUBSTRATE COMPLEX; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; LYSOSOME; MAJOR HISTOCOMPATIBILITY COMPLEX; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; UBIQUITINATION; BACTERIAL MEMBRANE; BIOSYNTHESIS; CELL MEMBRANE; CELL SEPARATION; CONFOCAL MICROSCOPY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HELA CELL; IMMUNOBLOTTING; IMMUNOLOGY; IMMUNOPRECIPITATION; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANTIGENS, CD; ANTIGENS, VIRAL; BACTERIAL CAPSULES; CELL ADHESION MOLECULES; CELL MEMBRANE; CELL SEPARATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HELA CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; SIGNAL TRANSDUCTION; TRANSFECTION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 77953628954     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0904154     Document Type: Article

References (48)

1. Peaper, D. R., and P. Cresswell. 2008. Regulation of MHC class I assembly and peptide binding. Annu. Rev. Cell Dev. Biol. 24: 343-368.
2. Radhakrishna, H., and J. G. Donaldson. 1997. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139: 49-61.
3. Naslavsky, N., R. Weigert, and J. G. Donaldson. 2004. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol. Biol. Cell 15: 3542-3552.
4. Lehner, P. J., S. Hoer, R. Dodd, and L. M. Duncan. 2005. Downregulation of cell surface receptors by the K3 family of viral and cellular ubiquitin E3 ligases. Immunol. Rev. 207: 112-125.
5. Coscoy, L., D. J. Sanchez, and D. Ganem. 2001. A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition. J. Cell Biol. 155: 1265-1273. (Pubitemid 34286275)
6. Ishido, S., C. Wang, B. S. Lee, G. B. Cohen, and J. U. Jung. 2000. Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J. Virol. 74: 5300-5309.
7. Hewitt, E. W., L. Duncan, D. Mufti, J. Baker, P. G. Stevenson, and P. J. Lehner. 2002. Ubiquitylation of MHC class I by the K3 viral protein signals internalization and TSG101-dependent degradation. EMBO J. 21: 2418-2429.
8. Duncan, L. M., S. Piper, R. B. Dodd, M. K. Saville, C. M. Sanderson, J. P. Luzio, and P. J. Lehner. 2006. Lysine-63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J. 25: 1635-1645.
9. Huang, F., D. Kirkpatrick, X. Jiang, S. Gygi, and A. Sorkin. 2006. Differential regulation of EGF receptor internalization and degradation by multi-ubiquitination within the kinase domain. Mol. Cell 21: 737-748. (Pubitemid 43376125)
10. Ohmura-Hoshino, M., Y. Matsuki, M. Mito-Yoshida, E. Goto, M. Aoki-Kawasumi, M. Nakayama, O. Ohara, and S. Ishido. 2009. Cutting edge: requirement of MARCH-I-mediated MHC II ubiquitination for the maintenance of conventional dendritic cells. J. Immunol. 183: 6893-6897.
11. Nathan, J. A., and P. J. Lehner. 2009. The trafficking and regulation of membrane receptors by the RING-CH ubiquitin E3 ligases. Exp. Cell Res. 315: 1593-1600.
12. Lorick, K. L., J. P. Jensen, S. Fang, A. M. Ong, S. Hatakeyama, and A. M. Weissman. 1999. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl. Acad. Sci. USA 96: 11364-11369.
13. Deshaies, R. J., and C. A. Joazeiro. 2009. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78: 399-434.
14. Eletr, Z. M., D. T. Huang, D. M. Duda, B. A. Schulman, and B. Kuhlman. 2005. E2 conjugating enzymes must disengage from their E1 enzymes before E3-dependent ubiquitin and ubiquitin-like transfer. Nat. Struct. Mol. Biol. 12: 933-934.
15. Markson, G., C. Kiel, R. Hyde, S. Brown, P. Charalabous, A. Bremm, J. Semple, J. Woodsmith, S. Duley, K. Salehi-Ashtiani, et al. 2009. Analysis of the human E2 ubiquitin conjugating enzyme protein interaction network. Genome Res. 19: 1905-1911.
16. van Wijk, S. J., S. J. de Vries, P. Kemmeren, A. Huang, R. Boelens, A. M. Bonvin, and H. T. Timmers. 2009. A comprehensive framework of E2-RING E3 interactions of the human ubiquitin-proteasome system. Mol. Syst. Biol. 5: 295.
17. Brzovic, P. S., J. R. Keeffe, H. Nishikawa, K. Miyamoto, D. Fox, 3rd, M. Fukuda, T. Ohta, and R. Klevit. 2003. Binding and recognition in the assembly of an active BRCA1/BARD1 ubiquitin-ligase complex. Proc. Natl. Acad. Sci. USA 100: 5646-5651.
18. Christensen, D. E., P. S. Brzovic, and R. E. Klevit. 2007. E2-BRCA1 RING interactions dictate synthesis of mono- or specific polyubiquitin chain linkages. Nat. Struct. Mol. Biol. 14: 941-948.
19. VanDemark, A. P., R. M. Hofmann, C. Tsui, C. M. Pickart, and C. Wolberger. 2001. Molecular insights into polyubiquitin chain assembly: crystal structure of the Mms2/Ubc13 heterodimer. Cell 105: 711-720.
20. Ikeda, F., and I. Dikic. 2008. Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: Beyond the Usual Suspects' review series. EMBO Rep. 9: 536-542.
21. Galan, J. M., and R. Haguenauer-Tsapis. 1997. Ubiquitin lys63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO J. 16: 5847-5854.
22. Kumar, K. G., H. Barriere, C. J. Carbone, J. Liu, G. Swaminathan, P. Xu, Y. Li, D. P. Baker, J. Peng, G. L. Lukacs, and S. Y. Fuchs. 2007. Site-specific ubiquitination exposes a linear motif to promote interferon-alpha receptor endocytosis. J. Cell Biol. 179: 935-950.
23. Geetha, T., J. Jiang, and M. W. Wooten. 2005. Lysine 63 polyubiquitination of the nerve growth factor receptor TrkA directs internalization and signaling. Mol. Cell 20: 301-312.
24. Kamsteeg, E. J., G. Hendriks, M. Boone, I. B. Konings, V. Oorschot, P. van der Sluijs, J. Klumperman, and P. M. Deen. 2006. Short-chain ubiquitination mediates the regulated endocytosis of the aquaporin-2 water channel. Proc. Natl. Acad. Sci. USA 103: 18344-18349.
25. Varghese, B., H. Barriere, C. J. Carbone, A. Banerjee, G. Swaminathan, A. Plotnikov, P. Xu, J. Peng, V. Goffin, G. L. Lukacs, and S. Y. Fuchs. 2008. Polyubiquitination of prolactin receptor stimulates its internalization, post-internalization sorting, and degradation via the lysosomal pathway. Mol. Cell. Biol. 28: 5275-5287.
26. Hicke, L., H. L. Schubert, and C. P. Hill. 2005. Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 6: 610-621.
27. Tsirigotis, M., M. Zhang, R. K. Chiu, B. G. Wouters, and D. A. Gray. 2001. Sensitivity of mammalian cells expressing mutant ubiquitin to protein-damaging agents. J. Biol. Chem. 276: 46073-46078.
28. Coscoy, L., and D. Ganem. 2001. A viral protein that selectively downregulates ICAM-1 and B7-2 and modulates T cell costimulation. J. Clin. Invest. 107: 1599-1606.
29. Ishido, S., J. K. Choi, B. S. Lee, C. Wang, M. DeMaria, R. P. Johnson, G. B. Cohen, and J. U. Jung. 2000. Inhibition of natural killer cell-mediated cytotoxicity by Kaposi's sarcoma-associated herpesvirus K5 protein. Immunity 13: 365-374.
30. Hofmann, R. M., and C. M. Pickart. 1999. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96: 645-653.
31. Deng, L., C. Wang, E. Spencer, L. Yang, A. Braun, J. You, C. Slaughter, C. Pickart, and Z. J. Chen. 2000. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103: 351-361.
32. McKenna, S., L. Spyracopoulos, T. Moraes, L. Pastushok, C. Ptak, W. Xiao, and M. J. Ellison. 2001. Noncovalent interaction between ubiquitin and the human DNA repair protein Mms2 is required for Ubc13-mediated polyubiquitination. J. Biol. Chem. 276: 40120-40126.
33. McKenna, S., T. Moraes, L. Pastushok, C. Ptak, W. Xiao, L. Spyracopoulos, and M. J. Ellison. 2003. An NMR-based model of the ubiquitin-bound human ubiquitin conjugation complex Mms2.Ubc13. The structural basis for lysine 63 chain catalysis. J. Biol. Chem. 278: 13151-13158.
34. Eddins, M. J., C. M. Carlile, K. M. Gomez, C. M. Pickart, and C. Wolberger. 2006. Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat. Struct. Mol. Biol. 13: 915-920.
35. Tsui, C., A. Raguraj, and C. M. Pickart. 2005. Ubiquitin binding site of the ubiquitin E2 variant (UEV) protein Mms2 is required for DNA damage tolerance in the yeast RAD6 pathway. J. Biol. Chem. 280: 19829-19835.
36. Xie, Y., and A. Varshavsky. 1999. The E2-E3 interaction in the N-end rule pathway: the RING-H2 finger of E3 is required for the synthesis of multi-ubiquitin chain. EMBO J. 18: 6832-6844.
37. Chen, B., J. Mariano, Y. C. Tsai, A. H. Chan, M. Cohen, and A. M. Weissman. 2006. The activity of a human endoplasmic reticulum-associated degradation E3, gp78, requires its Cue domain, RING finger, and an E2-binding site. Proc. Natl. Acad. Sci. USA 103: 341-346.
38. Ozkan, E., H. Yu, and J. Deisenhofer. 2005. Mechanistic insight into the allosteric activation of a ubiquitin-conjugating enzyme by RING-type ubiquitin ligases. Proc. Natl. Acad. Sci. USA 102: 18890-18895.
39. Siepmann, T. J., R. N. Bohnsack, Z. Tokgöz, O. V. Baboshina, and A. L. Haas. 2003. Protein interactions within the N-end rule ubiquitin ligation pathway. J. Biol. Chem. 278: 9448-9457.
40. van den Elsen, P. J., T. M. Holling, H. F. Kuipers, and N. van der Stoep. 2004. Transcriptional regulation of antigen presentation. Curr. Opin. Immunol. 16: 67-75.
41. Tourdot, S., M. Nejmeddine, S. J. Powis, and K. G. Gould. 2005. Different MHC class I heavy chains compete with each other for folding independently of beta 2-microglobulin and peptide. J. Immunol. 174: 925-933.
42. Knittler, M. R., K. Gülow, A. Seelig, and J. C. Howard. 1998. MHC class I molecules compete in the endoplasmic reticulum for access to transporter associated with antigen processing. J. Immunol. 161: 5967-5977.
43. Tussey, L. G., S. Rowland-Jones, T. S. Zheng, M. J. Androlewicz, P. Cresswell, J. A. Frelinger, and A. J. McMichael. 1995. Different MHC class I alleles compete for presentation of overlapping viral epitopes. Immunity 3: 65-77.
44. Boname, J. M., M. Thomas, H. R. Stagg, P. Xu, J. Peng, and P. J. Lehner. 2010. Efficient internalization of MHC I requires lysine-11 and lysine-63 mixed linkage polyubiquitin chains. Traffic 11: 210-220.
45. Cadwell, K., and L. Coscoy. 2005. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309: 127-130.
46. Matsuki, Y., M. Ohmura-Hoshino, E. Goto, M. Aoki, M. Mito-Yoshida, M. Uematsu, T. Hasegawa, H. Koseki, O. Ohara, M. Nakayama, et al. 2007. Novel regulation of MHC class II function in B cells. EMBO J. 26: 846-854. (Pubitemid 46253856)
47. Bartee, E., M. Mansouri, B. T. Hovey Nerenberg, K. Gouveia, and K. Früh. 2004. Downregulation of major histocompatibility complex class I by human ubiquitin ligases related to viral immune evasion proteins. J. Virol. 78: 1109-1120. (Pubitemid 38095821)
48. Hoer, S., L. Smith, and P. J. Lehner. 2007. MARCH-IX mediates ubiquitination and downregulation of ICAM-1. FEBS Lett. 581: 45-51.